Filarial Worms Reduce Plasmodium Infectivity in Mosquitoes

Matthew T Aliota,Jeremy F Fuchs,Henry Dagoro,Cheng-Chen Chen,Bruce M Christensen,Rhoel Ramos Dinglasan

doi:10.1371/journal.pntd.0000963

Abstract

BackgroundCo-occurrence of malaria and filarial worm parasites has been reported, but little is known about the interaction between filarial worm and malaria parasites with the same Anopheles vector. Herein, we present data evaluating the interaction between Wuchereria bancrofti and Anopheles punctulatus in Papua New Guinea (PNG). Our field studies in PNG demonstrated that An. punctulatus utilizes the melanization immune response as a natural mechanism of filarial worm resistance against invading W. bancrofti microfilariae. We then conducted laboratory studies utilizing the mosquitoes Armigeres subalbatus and Aedes aegypti and the parasites Brugia malayi, Brugia pahangi, Dirofilaria immitis, and Plasmodium gallinaceum to evaluate the hypothesis that immune activation and/or development by filarial worms negatively impact Plasmodium development in co-infected mosquitoes. Ar. subalbatus used in this study are natural vectors of P. gallinaceum and B. pahangi and they are naturally refractory to B. malayi (melanization-based refractoriness).Methodology/Principal FindingsMosquitoes were dissected and Plasmodium development was analyzed six days after blood feeding on either P. gallinaceum alone or after taking a bloodmeal containing both P. gallinaceum and B. malayi or a bloodmeal containing both P. gallinaceum and B. pahangi. There was a significant reduction in the prevalence and mean intensity of Plasmodium infections in two species of mosquito that had dual infections as compared to those mosquitoes that were infected with Plasmodium alone, and was independent of whether the mosquito had a melanization immune response to the filarial worm or not. However, there was no reduction in Plasmodium development when filarial worms were present in the bloodmeal (D. immitis) but midgut penetration was absent, suggesting that factors associated with penetration of the midgut by filarial worms likely are responsible for the observed reduction in malaria parasite infections.Conclusions/SignificanceThese results could have an impact on vector infection and transmission dynamics in areas where Anopheles transmit both parasites, i.e., the elimination of filarial worms in a co-endemic locale could enhance malaria transmission.

Highlights

Malaria and lymphatic filariasis (LF) are two of the most important mosquito-borne diseases
Human LF is caused by several species of mosquito-borne filarial nematodes, including Brugia malayi, Brugia timori, and Wuchereria bancrofti, but W. bancrofti is responsible for 90% of LF infections worldwide
LF is rarely fatal, severe morbidity occurs in 40% of infected individuals and involves disfigurement of the limbs and male genitalia [2,3,4]. Both malaria and LF are coendemic in many areas of the tropics and in certain areas are transmitted by the same Anopheles mosquitoes [5,6,7]

Summary

Introduction

Malaria and lymphatic filariasis (LF) are two of the most important mosquito-borne diseases. LF is rarely fatal, severe morbidity (including adverse economic and psychosexual effects) occurs in 40% of infected individuals and involves disfigurement of the limbs and male genitalia (elephantiasis and hydrocele, respectively) [2,3,4] Both malaria and LF are coendemic in many areas of the tropics and in certain areas are transmitted by the same Anopheles mosquitoes [5,6,7]. Co-infection of multiple species of malaria parasites or a combination of malaria and filarial worm parasites in humans have been reported [7,8], and in some cases can be quite frequent [9] Mixed infections of these two parasites within individual mosquitoes can occur in areas where more than one species of parasite is endemic and where Anopheles mosquitoes transmit both Plasmodium and filarial worm parasites, e.g., Papua New Guinea (PNG), rural sub-Saharan Africa, Asia, etc. Ar. subalbatus used in this study are natural vectors of P. gallinaceum and B. pahangi and they are naturally refractory to B. malayi (melanization-based refractoriness)

Methods

Results

Conclusion