Mosquitoes as Potential Bridge Vectors of Malaria Parasites from Non-Human Primates to Humans

Malaria is caused by Plasmodium parasites which are transmitted by mosquitoes. Until recently, human malaria was considered to be caused by human-specific Plasmodium species. Studies on Plasmodium parasites in non-human primates (NHPs), however, have identified parasite species in gorillas and chimpanzees that are closely related to human Plasmodium species. Moreover, P. knowlesi, long known as a parasite of monkeys, frequently infects humans. The requirements for such a cross-species exchange and especially the role of mosquitoes in this process are discussed, as the latter may act as bridge vectors of Plasmodium species between different primates. Little is known about the mosquito species that would bite both humans and NHPs and if so, whether humans and NHPs share the same Plasmodium vectors. To understand the vector-host interactions that can lead to an increased Plasmodium transmission between species, studies are required that reveal the nature of these interactions. Studying the potential role of NHPs as a Plasmodium reservoir for humans will contribute to the ongoing efforts of human malaria elimination, and will help to focus on critical areas that should be considered in achieving this goal

Design of trials for interrupting the transmission of endemic pathogens

Many interventions against infectious diseases have geographically diffuse effects. This leads to contamination between arms in cluster-randomized trials (CRTs). Pathogen elimination is the goal of many intervention programs against infectious agents, but contamination means that standard CRT designs and analyses do not provide inferences about the potential of interventions to interrupt pathogen transmission at maximum scale-up.; A generic model of disease transmission was used to simulate infections in stepped wedge cluster-randomized trials (SWCRTs) of a transmission-reducing intervention, where the intervention has spatially diffuse effects. Simulations of such trials were then used to examine the potential of such designs for providing generalizable causal inferences about the impact of such interventions, including measurements of the contamination effects. The simulations were applied to the geography of Rusinga Island, Lake Victoria, Kenya, the site of the SolarMal trial on the use of odor-baited mosquito traps to eliminate Plasmodium falciparum malaria. These were used to compare variants in the proposed SWCRT designs for the SolarMal trial.; Measures of contamination effects were found that could be assessed in the simulated trials. Inspired by analyses of trials of insecticide-treated nets against malaria when applied to the geography of the SolarMal trial, these measures were found to be robust to different variants of SWCRT design. Analyses of the likely extent of contamination effects supported the choice of cluster size for the trial.; The SWCRT is an appropriate design for trials that assess the feasibility of local elimination of a pathogen. The effects of incomplete coverage can be estimated by analyzing the extent of contamination between arms in such trials, and the estimates also support inferences about causality. The SolarMal example illustrates how generic transmission models incorporating spatial smoothing can be used to simulate such trials for a power calculation and optimization of cluster size and randomization strategies. The approach is applicable to a range of infectious diseases transmitted via environmental reservoirs or via arthropod vectors

Autodissemination of the entomopathogenic fungus Metarhizium anisopliae amongst adults of the malaria vector Anopheles gambiae s.s.

BACKGROUND: The entomopathogenic fungus Metarhizium anisopliae is being considered as a biocontrol agent for adult African malaria vectors. In the laboratory, work was carried out to assess whether horizontal transmission of the pathogen can take place during copulation, as this would enhance the impact of the fungus on target populations when compared with insecticides. METHODS: Virgin female Anopheles gambiae sensu stricto were exposed to conidia whilst resting on fungus-impregnated paper. These females were then placed together for one hour with uncontaminated males in proportions of either 1:1 or 1:10 shortly before the onset of mating activity. RESULTS: Males that had acquired fungal infection after mating indicate that passive transfer of the pathogen from infected females does occur, with mean male infection rates between 10.7 ± 3.2% and 33.3 ± 3.8%. The infections caused by horizontal transmission did not result in overall differences in survival between males from test and control groups, but in one of the three experiments the infected males had significantly shorter life spans than uninfected males (P < 0.05). CONCLUSION: This study shows that autodissemination of fungal inoculum between An. gambiae s.s. mosquitoes during mating activity is possible under laboratory conditions. Field studies are required next, to assess the extent to which this phenomenon may augment the primary contamination pathway (i.e. direct contact with fungus-impregnated targets) of vector populations in the field

Host-specific cues cause differential attractiveness of Kenyan men to the African malaria vector Anopheles gambiae

BACKGROUND: Many studies have suggested that variability in the attractiveness of humans to host-seeking mosquitoes is caused by differences in the make-up of body emanations, and olfactory signals in particular. Most investigations have either been laboratory-based, utilising odour obtained from sections of the body, or have been done in the field with sampling methods that do not discriminate between visual, physical and chemical cues of the host. Accordingly, evidence for differential attractiveness based on body emanations remains sparse in spite of the far-reaching epidemiological implications of this phenomenon. METHODS: A new three-port olfactometer that accommodates complete human beings as sources of host-seeking stimuli was used to study behavioural responses of Anopheles gambiae Giles sensu stricto (hereafter An. gambiae) under semi-field conditions in western Kenya. Differential attractiveness of nine male Kenyans was assessed by simultaneously exposing the mosquitoes to (a mixture of) total body emanations of 3 people occupying separate tents. Controls (empty tents) were included and the effect of residual odours following tent occupation was also examined. RESULTS: Trap catches increased significantly (P < 0.001) when a tent was occupied. Based on 'competition' experiments, the nine persons were classified into least, medium and most attractive groups. There was no significant interaction between person and trap (P = 0.302) or person and test period (P = 0.223). Presence (P < 0.001) or absence (P = 0.949) of significant differences in the number of mosquitoes caught per trap when tents were simultaneously occupied by one person in each or left empty, respectively, demonstrated that residual odours following tent occupation did not affect behavioural responses of the mosquitoes. CONCLUSION: We provide evidence that in the vicinity of humans, when exposed to a blend of physical and olfactory signals from more than one host, An. gambiae can effectively and consistently express host-selection behaviour that results in non-random biting

Evaluation of textile substrates for dispensing synthetic attractants for malaria mosquitoes

Background: The full-scale impact of odour-baited technology on the surveillance, sampling and control of vectors of infectious diseases is partly limited by the lack of methods for the efficient and sustainable dispensing of attractants. In this study we investigated whether locally-available and commonly used textiles are efficient substrates for the release of synthetic odorant blends attracting malaria mosquitoes. Methods: The relative efficacy of (a) polyester, (b) cotton, (c) cellulose + polyacrylate, and (d) nylon textiles as substrates for dispensing a synthetic odour blend (Ifakara blend 1(IB1)) that attracts malaria mosquitoes was evaluated in western Kenya. The study was conducted through completely randomized Latin square experimental designs under semi-field and field conditions. Results: Traps charged with IB1-impregnated polyester, cotton and cellulose + polyacrylate materials caught significantly more female Anopheles gambiae sensu stricto (semi-field conditions) and An. gambiae sensu lato (field conditions) mosquitoes than IB1-treated nylon (P = 0.001). The IB1-impregnated cellulose + polyacrylate material was the most attractive to female An. funestus mosquitoes compared to all other dispensing textile substrates (P < 0.001). The responses of female An. funestus mosquitoes to IB1-treated cotton and polyester were equal (P = 0.45). Significantly more female Culex mosquitoes were attracted to IB1-treated cotton than to the other treatments (P < 0.001). Whereas IB1-impregnated cotton and cellulose + polyacrylate material attracted equal numbers of female Mansonia mosquitoes (P = 0.44), the catches due to these two substrates were significantly higher than those associated with the other substrates (P < 0.001). Conclusion: The number and species of mosquitoes attracted to a synthetic odour blend is influenced by the type of odour-dispensing material used. Thus, surveillance and intervention programmes for malaria and other mosquito vectors using attractive odour baits should select an odour-release material that optimizes the odour blend

Trapping of the malaria vector Anopheles gambiae with odour-baited MM-X traps in semi-field conditions in western Kenya

BACKGROUND: The successful development of odour-baited trapping systems for mosquitoes depends on the identification of behaviourally active semiochemicals, besides the design and operating principles of such devices. A large variety of 'attractants' has been identified in laboratory investigations, yet few of these increase trap catches in the field. A contained system, intermediate between the laboratory and open field, is presented and previous reports that human foot odour induces behavioural responses of Anopheles gambiae confirmed. METHODS: The response of 3–5 day old female An. gambiae towards odour-baited counterflow geometry traps (MM-X model; American Biophysics Corp., RI) was studied in semi-field (screen house) conditions in western Kenya. Traps were baited with human foot odour (collected on socks), carbon dioxide (CO(2), 500 ml min(-1)), ammonia (NH(3)), 1-octen-3-ol, or various combinations thereof. Trap catches were log (x+1) transformed and subjected to Latin square analysis of variance procedures. RESULTS: Apart from 1-octen-3-ol, all odour baits caused significant (P < 0.05) increases in trap catches over non-baited traps. Foot odour remained behaviourally active for at least 8 days after collection on nylon or cotton sock fabric. A synergistic response (P < 0.001) was observed towards the combination of foot odour and CO(2), which increased catches of these odours alone by 3.8 and 2.7 times, respectively. CONCLUSION: These results are the first to report behavioural responses of an African malaria vector to human foot odour outside the laboratory, and further investigation of fractions and/or individual chemical components of this odour complex are called for. Semi-field systems offer the prospect of high-throughput screening of candidate kairomones, which may expedite the development of efficient trap-bait systems for this and other African mosquito species

Efficacy of Aquatain, a Monomolecular Film, for the Control of Malaria Vectors in Rice Paddies

Background Rice paddies harbour a large variety of organisms including larvae of malaria mosquitoes. These paddies are challenging for mosquito control because their large size, slurry and vegetation make it difficult to effectively apply a control agent. Aquatain, a monomolecular surface film, can be considered a suitable mosquito control agent for such breeding habitats due to its physical properties. The properties allow Aquatain to self-spread over a water surface and affect multiple stages of the mosquito life cycle. Methodology/Principal Findings A trial based on a pre-test/post-test control group design evaluated the potential of Aquatain as a mosquito control agent at Ahero rice irrigation scheme in Kenya. After Aquatain application at a dose of 2 ml/m2 on rice paddies, early stage anopheline larvae were reduced by 36%, and late stage anopheline larvae by 16%. However, even at a lower dose of 1 ml/m2 there was a 93.2% reduction in emergence of anopheline adults and 69.5% reduction in emergence of culicine adults. No pupation was observed in treated buckets that were part of a field bio-assay carried out parallel to the trial. Aquatain application saved nearly 1.7 L of water in six days from a water surface of 0.2 m2 under field conditions. Aquatain had no negative effect on rice plants as well as on a variety of non-target organisms, except backswimmers. Conclusions/Significance We demonstrated that Aquatain is an effective agent for the control of anopheline and culicine mosquitoes in irrigated rice paddies. The agent reduced densities of aquatic larval stages and, more importantly, strongly impacted the emergence of adult mosquitoes. Aquatain also reduced water loss due to evaporation. No negative impacts were found on either abundance of non-target organisms, or growth and development of rice plants. Aquatain, therefore, appears a suitable mosquito control tool for use in rice agro-ecosystems

Essential oils of Tagetes minuta and Tithonia diversifolia affect host location behaviour and on-host attachment site preference of the brown ear tick, Rhipicephalus appendiculatus in the semi-field studies

Effects of essential oils of Tagetes minuta and Tithonia diversifolia (Asteraceae) on orientation behaviour and on-host attachment site preference of newly hatched adult Rhipicephalus appendiculatus were evaluated. Host animals were treated at the ear pinna (by smearing the oil directly on the ear or suspending a tube containing the oil on the ear pinna) and legs + tail in semi-field plots. The legs + tail sites of the essential oil application showed the lowest mean percentage of ticks observed on host body (16.5 ± 1.9% and 26.0 ± 2.8%) and the highest mean percentage reduction of attaching ticks (76.5 ± 3.9% and 67.0 ± 0.8%) for essential oils of Tagetes minuta and Tithonia diversifolia, respectively. The control animals had the highest mean percentage of ticks observed (93.0 ± 2.1%). The ear tube resulted in the highest mean percentage of ticks on the host (47.5 ± 5.1% and 55.8 ± 5.1%) and a lowest mean percentage reduction of attaching ticks (44.8 ± 5.1% and 36.5 ± 7.4%) for the essential oils of Tagetes minuta and Tithonia diversifolia, respectively. For both the essential oils, legs + tail sites of essential oil application, followed by ear smear and then ear tube, had significant effects on orientation to the host and attachment site preference of adult R. appendiculatus on the host, in that order. We, therefore, recommend the ear smear site for treating hosts with essential oils whose performance may improve upon increasing concentration and formulating them in a carrier material that stabilizes the active ingredients