Plasmodium falciparum gametocyte-induced volatiles enhance attraction of Anopheles mosquitoes in the field

Abstract

Background: Plasmodium parasites manipulate the interaction between their mosquito and human hosts. Patients infected with gametocytes attract anopheline mosquitoes differentially compared to healthy individuals, an effect associated with an increased release of attractive volatile cues. This odour-driven manipulation is partly mediated by the gametocyte-specific metabolite, (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP), which induces increased release of select aldehydes and terpenes from red blood cells and results in the enhanced attraction of host-seeking mosquitoes, which are vectors of malaria. This study investigates the effect of the HMBPP-induced volatiles on the attraction of wild Anopheles mosquitoes to humans under field conditions. Methods: The efficacy of the HMBPP-induced odour blend to attract Anopheles was evaluated in a 4 × 6 Latin rectangular study design indoors using baited Suna traps. Furthermore, to assess the efficacy of the HMBPP-induced odour blend in (1) augmenting the attractiveness of human odour, and (2) attracting Anopheles mosquitoes in the absence of human odour, a two-choice assay using host decoy traps (HDTs) was used and evaluated using binomial generalized regression. Results: Traps baited with the HMBPP-induced odour blend attracted and caught both Anopheles arabiensis and Anopheles pharoensis females in a dose-dependent manner in the presence of background human odour, up to 2.5 times that of an unbaited trap. Given a choice between human odour and human odour laden with the HMBPPinduced odour blend, mosquitoes differentially preferred traps augmented with the HMBPP-induced odour blend, which caught twice as many female An. arabiensis. Traps baited with the HMBPP-induced odour blend but lacking the background of human odour were not effective in attracting and catching mosquitoes. Conclusion: The findings of the present study revealed that the HMBPP-induced odour blend, when augmented with human body odour, is attractive to anopheline mosquitoes and could be used as a complementary vector control tool along with existing strategies.

Mosquito Salivary Antigens and their Relationship to Dengue and P. <em>vivax </em>Malaria

“…Indeed, among our DENV-infected participants, we observed a significant positive correlation between RBC and both Nterm34kDa and gSG6-P1 peptides, suggesting increased exposure to mosquito bites while infected. Moreover, a recent study suggested that infection with DENV increased attractiveness to Aedes mosquitoes 52 , similar to observations made with Anopheles mosquitoes and Plasmodium gametocyte carriers 39,42 .…”

“…In malaria, Plasmodium gametocytes in vertebrate blood are the infectious stages for the mosquito vector. Interestingly, previous studies showed that the carriage of specific parasite stages influenced host attractiveness to mosquitoes, with people that harbored gametocytes in their blood being more attractive to mosquitoes than those presenting parasitemia with only asexual stages 39,40,41,42 . Here, we evaluated gametocyte carriage by measuring the expression of Plasmodium vivax Pvs25, while Pvs230 was used to determine gametocyte carriage 43,44 .…”

Variability in human attractiveness to mosquitoes

“…To the best of our knowledge, this is the more consistent evidence on how malaria infection can increase the human attractiveness to mosquitoes. More recently, Debebe et al. (2020) showed that HMBPP-induced volatiles indeed can attract Anopheles mosquitoes under field conditions.…”

The Potential Use of Volatile Biomarkers for Malaria Diagnosis

“…Plasmodium gametocytes, the parasite’s transmissible stage, have been evidenced to influence the behavior of Anopheles mosquitoes. Gametocytes are able to double the attractiveness of gametocyte-infected patients to malaria vectors as compared to people who are parasite free, harbor asexual stages, or have gametocytes at submicroscopic densities, by changing the odor profile of these patients [ 52 , 53 ]. In the same study from Kenya, the presence of microscopic gametocytes was been linked to the emanation of ketone 2-octanone from infected individuals [ 50 ] ( Table 2 ).…”