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Human-to-mosquito transmission efficiency increases as malaria is controlled.

ABSTRACT: The efficiency of malaria transmission between human and mosquito has been shown to be influenced by many factors in the laboratory, although their impact in the field and how this changes with disease endemicity are unknown. Here we estimate how human-mosquito transmission changed as malaria was controlled in Dielmo, Senegal. Mathematical models were fit to data collected between 1990 and the start of vector control in 2008. Results show that asexual parasite slide prevalence in humans has reduced from 70 to 20%, but that the proportion of infectious mosquitoes has remained roughly constant. Evidence suggests that this is due to an increase in transmission efficiency caused by a rise in gametocyte densities, although the uneven distribution of mosquito bites between hosts could also contribute. The resilience of mosquito infection to changes in endemicity will have important implications for planning disease control, and the development and deployment of transmission-reducing interventions.

SUBMITTER: Churcher TS

PROVIDER: S-EPMC4309425 | biostudies-literature | 2015 Jan

REPOSITORIES: biostudies-literature

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Human-to-mosquito transmission efficiency increases as malaria is controlled.

Churcher Thomas S TS Trape Jean-François JF Cohuet Anna A

Nature communications 20150119

The efficiency of malaria transmission between human and mosquito has been shown to be influenced by many factors in the laboratory, although their impact in the field and how this changes with disease endemicity are unknown. Here we estimate how human-mosquito transmission changed as malaria was controlled in Dielmo, Senegal. Mathematical models were fit to data collected between 1990 and the start of vector control in 2008. Results show that asexual parasite slide prevalence in humans has redu ...[more]

PMID: 25597498

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Project description:Mating causes dramatic changes in female physiology, behaviour, and immunity in many insects, inducing oogenesis, oviposition, and refractoriness to further mating. Females from the Anopheles gambiae species complex typically mate only once in their lifetime during which they receive sperm and seminal fluid proteins as well as a mating plug that contains the steroid hormone 20-hydroxyecdysone. This hormone, which is also induced by blood-feeding, plays a major role in activating vitellogenesis for egg production. Here we show that female Anopheles coluzzii susceptibility to Plasmodium falciparum infection is significantly higher in mated females compared to virgins. We also find that mating status has a major impact on the midgut transcriptome, detectable only under sugar-fed conditions: once females have blood-fed, the transcriptional changes that are induced by mating are likely masked by the widespread effects of blood-feeding on gene expression. To determine whether increased susceptibility to parasites could be driven by the additional 20E that mated females receive from males, we mimicked mating by injecting virgin females with 20E, finding that these females are significantly more susceptible to human malaria parasites than virgin females injected with the control 20E carrier. Further RNAseq was carried out to examine whether the genes that change upon 20E injection in the midgut are similar to those that change upon mating. We find that 79 midgut-expressed genes are regulated in common by both mating and 20E, and 96% (n = 76) of these are regulated in the same direction (up vs down in 20E/mated). Together, these findings show that male Anopheles mosquitoes induce changes in the female midgut that can affect female susceptibility to P. falciparum. This implies that in nature, males might contribute to malaria transmission in previously unappreciated ways, and that vector control strategies that target males may have additional benefits towards reducing transmission.

Project description:BACKGROUND:Drugs and vaccines that can interrupt the transmission of Plasmodium falciparum will be important for malaria control and elimination. However, models for early clinical evaluation of candidate transmission-blocking interventions are currently unavailable. Here, we describe a new model for evaluating malaria transmission from humans to Anopheles mosquitoes using controlled human malaria infection (CHMI). METHODS:Seventeen healthy malaria-naive volunteers underwent CHMI by intravenous inoculation of P. falciparum-infected erythrocytes to initiate blood-stage infection. Seven to eight days after inoculation, participants received piperaquine (480 mg) to attenuate asexual parasite replication while allowing gametocytes to develop and mature. Primary end points were development of gametocytemia, the transmissibility of gametocytes from humans to mosquitoes, and the safety and tolerability of the CHMI transmission model. To investigate in vivo gametocytocidal drug activity in this model, participants were either given an experimental antimalarial, artefenomel (500 mg), or a known gametocytocidal drug, primaquine (15 mg), or remained untreated during the period of gametocyte carriage. RESULTS:Male and female gametocytes were detected in all participants, and transmission to mosquitoes was achieved from 8 of 11 (73%) participants evaluated. Compared with results in untreated controls (n = 7), primaquine (15 mg, n = 5) significantly reduced gametocyte burden (P = 0.01), while artefenomel (500 mg, n = 4) had no effect. Adverse events (AEs) were mostly mild or moderate. Three AEs were assessed as severe - fatigue, elevated alanine aminotransferase, and elevated aspartate aminotransferase - and were attributed to malaria infection. Transaminase elevations were transient, asymptomatic, and resolved without intervention. CONCLUSION:We report the safe and reproducible induction of P. falciparum gametocytes in healthy malaria-naive volunteers at densities infectious to mosquitoes, thereby demonstrating the potential for evaluating transmission-blocking interventions in this model. TRIAL REGISTRATION:ClinicalTrials.gov NCT02431637 and NCT02431650. FUNDING:Bill & Melinda Gates Foundation.

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Human-to-mosquito transmission efficiency increases as malaria is controlled.

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Human-to-mosquito transmission efficiency increases as malaria is controlled.

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