Mosquito-Parasite Interactions Can Shape Filariasis Transmission Dynamics and Impact Elimination Programs

Abstract

The relationship between mosquito vectors and lymphatic filariasis (LF) parasites can result in a range of transmission outcomes. Anophelines are generally characterized as poor vectors due to an inability to support development at low densities. However, it is important to understand the potential for transmission in natural vectors to maximize the success of elimination efforts. Primary vectors in Papua New Guinea (n = 1209) were dissected following exposure to microfilaremic blood (range 8–233 mf/20 µl). We examined density dependent and species-specific parasite prevalence, intensity and yield, barriers to parasite development as well as impacts on mosquito survival. We observed strikingly different parasite prevalence and yield among closely related species. Prevalence of infective stage larvae (L3s) ranged from 4.2% to 23.7% in An. punctulatus, 24.5% to 68.6% in An. farauti s.s. and 61.9% to 100% in An. hinesorum at low and high density exposures, respectively. Injection experiments revealed the greatest barrier to parasite development involved passage from the midgut into the hemocoel. The ratio of L3 to ingested mf at low densities was higher in An. hinesorum (yield = 1.0) and An. farauti s.s. (yield = 0.5) than has been reported in other anopheline vectors. There was a negative relationship between mosquito survival and bloodmeal mf density. In An. farauti s.s., increased parasite yield and survival at low densities suggest greater competence at low microfilaremias. In Papua New Guinea the likelihood of transmission will be strongly influenced by vector composition and changes in the mf reservoir as a result of elimination efforts. Global elimination efforts will be strengthened by the knowledge of transmission potential in the context of current control measures.

Filarial infection influences mosquito behaviour and fecundity

“…In nature, filariasis vector survival is known to be affected by parasite density8, however the strain of Aedes aegypti used in our study has been selected for susceptibility to Brugia malayi . With no significant differences in mortality between the various cohorts, and no significant differences in mean worm burden of dead and moribund mosquitoes, we conclude that density dependent mortality had no impact on our assay results.…”

“…Larval development occurs within the short lived mosquito and once transmitted to a vertebrate host, parasites carry out their longer life stages and reproduction5. Several different mosquito species from the Culex, Anopheles, Aedes and Mansonia genera can transmit LF4 but susceptibility to parasite infection varies between species678.…”

Molecular epidemiology, phylogeny and evolution of the filarial nematode Wuchereria bancrofti

“…Therefore, communities that are farther than the average flight distance should logically have little mixing of Wb by vector dispersal alone. Also only a small number of Wb worms are transported with each mosquito bite—on average 1–3 infective L3 larvae per mosquito (Erickson et al, 2013; Hairston and De Meillon, 1968). If we weigh this in contrast to human migration, whereas humans can easily move 2 Kilometers or more, and transport a whole population of Wb, we quickly determine that human migration will be more effective at dispersing Wb than vector dispersal.…”

Presence ofWuchereria bancroftimicrofilaremia despite 7 years of annual ivermectin monotherapy mass drug administration for onchocerciasis control: a study in north-west Ethiopia

“…24,25 As more mf are ingested by the mosquito, the cibarial armature's effect decreases as mf debris accumulates on the teeth, and by masking them to allow other mf to enter the vector unharmed. Once inside the vector, they may develop into infective larvae.…”