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.

Figure 1. The development of Wuchereria bancrofti from microfilaria to infective-stage larvae in Anopheles farauti s.s.

The number of parasites observed at each timepoint is listed above the bar.

Figure 2. Relationship between host mf density and the number of mf ingested.

Regression equations are not significantly different from each other (An. punctulatus Y = 0.045*X+0.22, An. farauti Y = 0.057*X-0.51; Slope: p = 0.5; Intercept: p = 0.89).

Figure 3. Attrition of developing W. bancrofti in multiple anopheline species from A) low B) medium and C) high microfilarial density blood.

The mean number of worms ingested (95% CI), including the proportion that were damaged upon ingestion by the cibarial armature, and the relative yield of developing worms (any stage, between 1 and 13 DPE) or the yield of L3s (between 13.5–18 DPE). Non-parametric t test compares mean number of intact mf with the mean number of developing worms, and the mean number of developing worms with the mean number of L3s (other stages present beyond 13.5DPE are not included in the mean). Bonferonni adjusted alpha for multiple comparisons = 0.004 *p<0.0001.

Figure 4. Attrition of developing W. bancrofti, incoluated into the hemocoel of A) An. farauti and B) An. punctulatus.

There was no significant difference between the mean number of parasites recovered immediately post-injection (<1 day) and the mean number of developing worms (recovered from 1.5–13 days post-injection).

Figure 5. Survival curves for An. farauti s.s. following exposure to different densities of microfilaremic blood.