Odours of Plasmodium falciparum-infected participants influence mosquito-host interactions

Jetske G De Boer,John C Caulfield,Robert W Sauerwein,Michael A Birkett,Willem Takken,Perry J J Van Genderen,John A Pickett,Saskia L G E Burgers,Ailie Robinson,Renate C Smallegange,Stephen J Powers,Teun Bousema,James G Logan

doi:10.1038/s41598-017-08978-9

Abstract

Malaria parasites are thought to influence mosquito attraction to human hosts, a phenomenon that may enhance parasite transmission. This is likely mediated by alterations in host odour because of its importance in mosquito host-searching behaviour. Here, we report that the human skin odour profile is affected by malaria infection. We compared the chemical composition and attractiveness to Anopheles coluzzii mosquitoes of skin odours from participants that were infected by Controlled Human Malaria Infection with Plasmodium falciparum. Skin odour composition differed between parasitologically negative and positive samples, with positive samples collected on average two days after parasites emerged from the liver into the blood, being associated with low densities of asexual parasites and the absence of gametocytes. We found a significant reduction in mosquito attraction to skin odour during infection for one experiment, but not in a second experiment, possibly due to differences in parasite strain. However, it does raise the possibility that infection can affect mosquito behaviour. Indeed, several volatile compounds were identified that can influence mosquito behaviour, including 2- and 3-methylbutanal, 3-hydroxy-2-butanone, and 6-methyl-5-hepten-2-one. To better understand the impact of our findings on Plasmodium transmission, controlled studies are needed in participants with gametocytes and higher parasite densities.

Highlights

Parasitic manipulation of hosts is found commonly, and is likely to have far-reaching consequences for disease ecology and epidemiology e.g
Skin odour collected after antimalarial treatment appeared to be less attractive than skin odour collected before malaria challenge, and in CHMI2, the odour profile of After samples separated from odour profiles of the other groups in the canonical variate analysis (CVA) (Supplementary Fig. S3), while there was a general trend for greater amounts of volatiles in After compared to before challenge (Before) samples
We observed changes in human skin odour profile during P. falciparum infection, on average two days after parasites moved from the liver to the peripheral blood, a phase that is characterized by low densities of asexual parasites[20, 33] and the absence of gametocytes, as was confirmed

Summary

Introduction

Parasitic manipulation of hosts is found commonly, and is likely to have far-reaching consequences for disease ecology and epidemiology e.g.1. We investigated whether P. falciparum infection affected skin odour profile of human participants in Controlled Human Malaria Infections (CHMI) and host-seeking behaviour of An. coluzzii mosquitoes. Both total volume and the constituent compounds (odour profile) of skin volatiles from CHMI participants were affected as early as 6–8 days after P. falciparum challenge, corresponding to on average 2 days after the parasites move from the liver to the blood.

Results

Conclusion