When Is a Plasmodium-Infected Mosquito an Infectious Mosquito?

Abstract

Plasmodium parasites experience significant bottlenecks as they transit through the mosquito and are transmitted to their mammalian host. Oocyst prevalence on mosquito midguts and sporozoite prevalence in salivary glands are nevertheless commonly used to confirm successful malaria transmission, assuming that these are reliable indicators of the mosquito's capacity to give rise to secondary infections. Here we discuss recent insights in sporogonic development and transmission bottlenecks for Plasmodium. We highlight critical gaps in our knowledge and frame their importance in understanding the human and mosquito reservoirs of infection. A better understanding of the events that lead to successful inoculation of infectious sporozoites by mosquitoes is critical to designing effective interventions to shrink the malaria map.

Keywords: Anopheles; gametocyte; mosquitoes; oocyst; salivary glands; sporozoite.

Figure 1:. Transmission bottlenecks in the Plasmodium life cycle.

(A) Estimated parasite numbers during the different life cycle stages reveals that transmission to and from the mosquito is associated with significant decreases in parasite numbers (meros, merozoites; spz, sporozoites; sg salivary gland; EEFs, exoerythrocytic forms). Adapted from Povelones et al [111]. (B) Specific bottlenecks faced by Plasmodium sporozoites: Cartoon of the sporozoites journey from mosquito to mammalian host, highlighting the following bottlenecks: #1 Estimates suggest ~20% of oocyst sporozoites reach the salivary glands; #2 Less than 1% of salivary gland sporozoites are expelled during probing; #3 ~20% of inoculated sporozoites enter the bloodstream; #4 represents several unmeasured bottlenecks, namely the efficiency with which sporozoite arrest in the liver, enter hepatocytes, and develop into liver stages. Artwork by Brandy Lee Bennett.

Figure 2:. Oocyst and sporozoite distributions in wild-caught mosquitoes.

Frequency distribution of (A) oocyst numbers and (B) salivary gland sporozoite numbers in wild-caught P. falciparum infected Anopheles gambiae mosquitoes (n=94). Adapted from Collins et al [71] with permission of the publisher.