Willem Takken

Host Preferences of Blood-Feeding Mosquitoes

Mosquitoes use plant sugars and vertebrate blood as nutritional resources. When searching for blood hosts, some mosquitoes express preferential behavior for selected species. Here, we review the available knowledge on host preference, as this is expected to affect the life history and transmission of infectious pathogens. Host preference is affected by myriad extrinsic and intrinsic factors. Inherent factors are determined by genetic selection, which appears to be controlled by adaptive advantages that result from feeding on certain host species. Host preference of mosquitoes, although having a genetic basis, is characterized by high plasticity mediated by the density of host species, which by their abundance form a readily accessible source of blood. Host-selection behavior in mosquitoes is an exception rather than the rule. Those species that express strong and inherent host-selection behavior belong to the most important vectors of infectious diseases, which suggests that this behavioral trait may have evolved in parallel with parasite-host evolution.

The Role of Olfaction in Host-Seeking of Mosquitoes: A Review

This review concentrates on air-borne chemical cues that blood-seeking mosquitoes use to locate a host. A distinction is made between short- and long-range attraction. Carbon dioxide is involved in both processes. It activates and attracts mosquitoes. The latter function is only observed in combination with an odorous organo-chemical. Other olfactory cues are primarily involved in long-range attraction. Bodily emanations from the host that contain olfactory cues can be divided into three groups: Skin emanations, exhaled air and urine. Each of these is attractive to mosquitoes, but there is little knowledge about the chemical compounds that cause the attraction. Lactic acid in the presence of CO2 is attractive, and lactic acid-sensitive neurosensilla are present on the antennae. Other host-produced chemicals are also attractive, but chemical identification and subsequent confirmation of attractiveness for mosquitoes has not been reported. Host preference in mosquitoes is speciesspecific and varies from highly specific to opportunistic. Attraction is likely to be caused by a mixture of several compounds. Synergism may be an important way of increasing the effect of separate chemical cues.RésuméCe rapport se concentre sur les facteurs chimiques volatils utilisés par les moustiques pour localiser un hôte nourricier. Une distinction est faite entre une attraction à courte et à longue distance. Le dioxyde de carbone est impliqué dans les deux cas, étant un activant et un attractif. Cette dernière fonction n’est impliquée qu’en combinaison avec un produit chimique olfactif. Les émanations corporelles d’un hôte nourricier contenant des facteurs volatils sont divisés en trois groupes:émanations de la peau, air expiré, et urine. Chaqu’un est attractif pour les moustiques, mais les produits chimiques responsables pour cette attraction sont peu connus. L’acid lactique en présence du dioxyde de carbon est attractif, et des neurosensilles sensibles à l’acid lactique se trouvent sur les antennes. D’autres produits chimiques venant d’hôtes nourriciers sont attractifs, mais leur identification et confirmation comme attractifs olfactifs n’a pas été rapportée. Chez les moustiques, la préférence alimentaire varie entre les espèces, de très spécifique à opportunistique. L’attraction est vraisemblablement due à un composé de produits chimiques. Une synergie pourrait augmenter l’effet de ces facteurs.

Malaria vector control: current and future strategies.

The recently announced call for malaria eradication represents a new page in the history of this disease. This has been triggered by remarkable reductions in malaria resulting from combined application of effective drugs and vector control. However, this strategy is threatened by development of insecticide resistance. Efforts to develop alternative tools to complement or even replace insecticide-based vector-control strategies must continue. Here, an overview is presented of the novel vector-control tools expected to contribute to malaria eradication.

Cultured skin microbiota attracts malaria mosquitoes

BackgroundHost-seeking of the African malaria mosquito, Anopheles gambiae sensu stricto, is guided by human odours. The precise nature of the odours, and the composition of attractive blends of volatiles, remains largely unknown. Skin microbiota plays an important role in the production of human body odours. It is hypothesized that host attractiveness and selection of An. gambiae is affected by the species composition, density, and metabolic activity of the skin microbiota. A study is presented in which the production and constituency of volatile organic compounds (VOCs) by human skin microbiota is examined and the behavioural responses of An. gambiae to VOCs from skin microbiota are investigated.MethodsBlood agar plates incubated with skin microbiota from human feet or with a reference strain of Staphylococcus epidermidis were tested for their attractiveness to An. gambiae in olfactometer bioassays and indoor trapping experiments. Entrained air collected from blood agar plates incubated with natural skin microbiota or with S. epidermidis were analysed using GC-MS. A synthetic blend of the compounds identified was tested for its attractiveness to An. gambiae. Behavioural data were analysed by a χ2-test and GLM. GC-MS results were analysed by fitting an exponential regression line to test the effect of the concentration of bacteria.ResultsMore An. gambiae were caught with blood agar plates incubated with skin bacteria than with sterile blood agar plates, with a significant effect of incubation time and dilution of the skin microbiota. When bacteria from the feet of four other volunteers were tested, similar effects were found. Fourteen putative attractants were found in the headspace of the skin bacteria. A synthetic blend of 10 of these was attractive to An. gambiae.ConclusionsThe discovery that volatiles produced by human skin microorganisms in vitro mediate An. gambiae host-seeking behaviour creates new opportunities for the development of odour-baited trapping systems. Additionally, identification of bacterial volatiles provides a new method to develop synthetic blends, attractive to An. gambiae and possibly other anthropophilic disease vectors.

Lessons from agriculture for the sustainable management of malaria vectors.

Willem Takken and colleagues argue for the expansion of insecticide monotherapy in malaria control by taking lessons from agriculture and including more sustainable integrated vector management strategies.

The effect of mass mosquito trapping on malaria transmission and disease burden (SolarMal): a stepped-wedge cluster-randomised trial

BACKGROUNDnOdour baits can attract host-seeking Anopheles mosquitoes indoors and outdoors. We assessed the effects of mass deployment of odour-baited traps on malaria transmission and disease burden.nnnMETHODSnWe installed solar-powered odour-baited mosquito trapping systems (SMoTS) to households on Rusinga Island, Lake Victoria, western Kenya (mean population 24u2008879), in a stepped-wedge cluster-randomised trial. All residents in the completed health and demographic surveillance system were eligible to participate. We used the travelling salesman algorithm to assign all households to a cluster (50 or 51 geographically contiguous households); nine contiguous clusters formed a metacluster. Initially, no cluster had SMoTS (non-intervened). During the course of the intervention roll-out SMoTS were gradually installed cluster by cluster until all clusters had SMoTS installed (intervened). We generated 27 cluster randomisations, with the cluster as unit of randomisation, to establish the order to install the traps in the clusters until all had a SMoTS installed. Field workers and participants were not masked to group allocation. The primary outcome of clinical malaria was monitored through repeated household visits covering the entire population, once before roll-out (baseline) and five times throughout the 2-year roll-out. We measured clinical malaria as fever plus a positive result with a rapid diagnostic test. The SolarMal project was registered on the Dutch Trial Register (NTR 3496).nnnFINDINGSnWe enrolled 34u2008041 participants between April 25, 2012, and March 23, 2015, to 81 clusters and nine metaclusters. 4358 households were provided with SMoTS during roll-out between June 3, 2013, and May 16, 2015. 23 clinical malaria episodes were recorded in intervened clusters and 33 episodes in non-intervened clusters (adjusted effectiveness 40·8% [95% CI -172·8 to 87·1], p=0·5) during the roll-out. Malaria prevalence measured by rapid diagnostic test was 29·8% (95% CI 20·9-38·0) lower in SMoTS clusters (prevalence 23·7%; 1552 of 6550 people) than in non-intervened clusters (prevalence 34·5%; 2002 of 5795 people).nnnINTERPRETATIONnThe unexpectedly low clinical incidence of malaria during roll-out led to an imprecise estimate of effectiveness from the clinical incidence data. The substantial effect on malaria prevalence is explained by reduction in densities of Anopheles funestus. Odour-baited traps might be an effective malaria intervention.nnnFUNDINGnCOmON Foundation.

West Nile Virus: High Transmission Rate in North-Western European Mosquitoes Indicates Its Epidemic Potential and Warrants Increased Surveillance

Background West Nile virus (WNV) is a highly pathogenic flavivirus transmitted by Culex spp. mosquitoes. In North America (NA), lineage 1 WNV caused the largest outbreak of neuroinvasive disease to date, while a novel pathogenic lineage 2 strain circulates in southern Europe. To estimate WNV lineage 2 epidemic potential it is paramount to know if mosquitoes from currently WNV-free areas can support further spread of this epidemic. Methodology/Principal Findings We assessed WNV vector competence of Culex pipiens mosquitoes originating from north-western Europe (NWE) in direct comparison with those from NA. We exposed mosquitoes to infectious blood meals of lineage 1 or 2 WNV and determined the infection and transmission rates. We explored reasons for vector competence differences by comparing intrathoracic injection versus blood meal infection, and we investigated the influence of temperature. We found that NWE mosquitoes are highly competent for both WNV lineages, with transmission rates up to 25%. Compared to NA mosquitoes, transmission rates for lineage 2 WNV were significantly elevated in NWE mosquitoes due to better virus dissemination from the midgut and a shorter extrinsic incubation time. WNV infection rates further increased with temperature increase. Conclusions/Significance Our study provides experimental evidence to indicate markedly different risk levels between both continents for lineage 2 WNV transmission and suggests a degree of genotype-genotype specificity in the interaction between virus and vector. Our experiments with varying temperatures explain the current localized WNV activity in southern Europe, yet imply further epidemic spread throughout NWE during periods with favourable climatic conditions. This emphasizes the need for intensified surveillance of virus activity in current WNV disease-free regions and warrants increased awareness in clinics throughout Europe.

Field Evaluation of a Push-Pull System to Reduce Malaria Transmission

Malaria continues to place a disease burden on millions of people throughout the tropics, especially in sub-Saharan Africa. Although efforts to control mosquito populations and reduce human-vector contact, such as long-lasting insecticidal nets and indoor residual spraying, have led to significant decreases in malaria incidence, further progress is now threatened by the widespread development of physiological and behavioural insecticide-resistance as well as changes in the composition of vector populations. A mosquito-directed push-pull system based on the simultaneous use of attractive and repellent volatiles offers a complementary tool to existing vector-control methods. In this study, the combination of a trap baited with a five-compound attractant and a strip of net-fabric impregnated with micro-encapsulated repellent and placed in the eaves of houses, was tested in a malaria-endemic village in western Kenya. Using the repellent delta-undecalactone, mosquito house entry was reduced by more than 50%, while the traps caught high numbers of outdoor flying mosquitoes. Model simulations predict that, assuming area-wide coverage, the addition of such a push-pull system to existing prevention efforts will result in up to 20-fold reductions in the entomological inoculation rate. Reductions of such magnitude are also predicted when mosquitoes exhibit a high resistance against insecticides. We conclude that a push-pull system based on non-toxic volatiles provides an important addition to existing strategies for malaria prevention.

A push-pull system to reduce house entry of malaria mosquitoes

BackgroundMosquitoes are the dominant vectors of pathogens that cause infectious diseases such as malaria, dengue, yellow fever and filariasis. Current vector control strategies often rely on the use of pyrethroids against which mosquitoes are increasingly developing resistance. Here, a push-pull system is presented, that operates by the simultaneous use of repellent and attractive volatile odorants.Method/ResultsExperiments were carried out in a semi-field set-up: a traditional house which was constructed inside a screenhouse. The release of different repellent compounds, para-menthane-3,8-diol (PMD), catnip oil e.o. and delta-undecalactone, from the four corners of the house resulted in significant reductions of 45% to 81.5% in house entry of host-seeking malaria mosquitoes. The highest reductions in house entry (up to 95.5%), were achieved by simultaneously repelling mosquitoes from the house (push) and removing them from the experimental set-up using attractant-baited traps (pull).ConclusionsThe outcome of this study suggests that a push-pull system based on attractive and repellent volatiles may successfully be employed to target mosquito vectors of human disease. Reductions in house entry of malaria vectors, of the magnitude that was achieved in these experiments, would likely affect malaria transmission. The repellents used are non-toxic and can be used safely in a human environment. Delta-undecalactone is a novel repellent that showed higher effectiveness than the established repellent PMD. These results encourage further development of the system for practical implementation in the field.

Evaluation of integrated vector management

Initiatives on integrated vector management (IVM) approaches are increasingly undertaken as alternatives to existing vector control. An impact model of IVM is presented with performance and impact indicators at six causal steps from coverage of the intervention to impact on disease. Impacts in fields other than health are also discussed because of the emphasis in IVM on capacity building, partnerships and sustainability. A conceptual framework for evaluation of IVM is designed, based on considerations of the selection of indicators, level of inference, cluster size and method of evaluation. The framework, which is tested in three case studies, is intended as guidance for public health workers and policy-makers.