Ecology of Disease Vectors

National Institute Of Allergy And Infectious Diseases

Investigators

Linked publications & trials

Abstract

With over a billion cases worldwide and a million deaths annually, vector borne diseases remain important globally. Malaria is prevalent worldwide with an especially heavy burden in Africa. Outstanding gaps remain in our understanding of the maintenance and spread of mosquito-borne pathogens within and from sylvatic cycles, limiting our success in disease prevention and control. 1. Our studies on aerial sampling of mosquitoes 40-290 m above the Sahel of Mali (Huestis et al. 2019: Nature, Yaro et al. 2022: Frontiers in Epidemiology) revealed regular activity of diverse mosquito species. Yet, the hypothesis that high-flying mosquitoes spread pathogens over long distances has not been directly tested. Our recent study (Bamou et al. 2024: Preprint) shows that high-flying windborne mosquitoes are commonly infected with arboviruses, protozoans, and helminths affecting vertebrates and humans, and provide the first description of this pathogen-vector aerial network. A total of 1,017 female mosquitoes intercepted on nets 120-290 m above ground over Mali and Ghana were screened for infection with arboviruses, plasmodia, and filariae. The mosquitoes collected at altitude comprised 61 species, across 10 genera, dominated by Culex, Aedes, and Anopheles. Infection and infectiousness (capacity to transmit a pathogen to another host inferred based on disseminated infection) rates of migrant mosquitoes were 7.2% and 4.4% with plasmodia, 1.6% and 0.6% with filariae, and 3.5% and 1.1% with flaviviruses, respectively. Twenty-one mosquito-borne pathogens were identified, including dengue, West Nile, and M’Poko viruses, 15 avian plasmodia species, and three filariid worms. Confirmed head-thorax (disseminated) infections of multiple pathogens in Culex perexiguus, Mansonia uniformis, and Anopheles squamosus reveal that pathogens carried by high-altitude windborne mosquitoes are capable of infecting hosts far from their departure location. This high-altitude traffic of sylvatic pathogens may be key to their maintenance among enzootic foci as well as initiating outbreaks at distant locations. Aerial surveillance could be used to map the sources and destinations of vectors and pathogens and thus mitigate public health threats. 2. To determine if high flying mosquitoes and other insects move across ecozones, we have expanded aerial sampling into the savannas ecozones (Mali) and into the woodland and equatorial forests (Ghana) as well as in Kenya (East Africa). In contrast to theoretical expectations, windborne mosquitoes occurred more commonly above perennial ecosystems including over the equatorial forests than above the Sahel. Based on species composition, movement between the equatorial forest to the Sahel >750 km may occur. A one-year study in Kenya has demonstrated that windborne mosquitoes and other insects are common across the continent (Atieli et al. 2023). 3. Mrs. Rita Nartey-Frimpong, a PhD student (joint NIH (GPP)- Kwame Nkrumah University of Science and Technology, Ghana) has been working on the insects collected at altitude in Mali and Ghana, focusing on species impacting food security. Invasive insects threaten ecosystem stability, public health, and food security. In her first paper (Nartey et al. 2024: Neobiota), Rita and colleagues report on the invasion of the South American leafhopper, Curtara insularis into Africa, where it has established populations in Ghana. Importantly, 80% of the specimens collected were intercepted between 160 and 190 m above ground and the fraction of this species among all insects collected was higher at altitude, demonstrating its propensity to engage in high-altitude windborne dispersal. Its aerial densities at altitude translate into millions of migrants/km over a year, representing massive invasive force (propagule pressure). To assess the contribution of windborne dispersal to its spread in a new territory, we examine records of C. insularis range-expansion in the USA. Reported first in 2004 from central Florida, it spread across the southeastern and south-central US. Its expansion fits a “diffusion-like” process with 200—300 km long “annual displacement steps”—a pattern consistent with autonomous dispersal rather than vehicular transport. Most “steps” are consistent with common wind trajectories from the nearest documented population, assuming 2—8 hours of wind-assisted flight at altitude. Curtara insularis has been intercepted at US ports and on trucks. Thus, it uses multiple dispersal modes, yet its rapid overland spread is best explained by its massive propagule pressure linked with its high-altitude windborne dispersal. We propose that high-altitude windborne dispersal is common yet under-appreciated in invasive insects. Currently Rita is based in Ghana, working to complete her thesis, focusing on a comparison of insect communities at altitude across ecozones. 4. In collaboration with Drs. Scott Weaver (UTMB USA) and Mawlouth Diallo (Institute Pasteur, Dakar), we initiated studies in Kedougou Senegal and Bantakoto Mali on windborne spread of arboviruses in mosquitoes. We compare aerial and ground samples of mosquitoes and pathogens over Kedougou, Senegal—a well-known hotspot for arbovirus activity that has been extensively studied for >50 years, with the Bantakoto aerial station across the border in Mali (110 km from Kedougou). In this project we address if arboviruses spread in windborne mosquitoes from enzootoic (sylvatic) cycles into new areas, generating outbreaks tens or hundreds of kilometers away. 5. In collaboration with Professors Diabate (IRSS, Burkina Faso), Dao (MRTC/UTTSB, Mali), Dadzie (Noguchi Institute/Univ. of Ghana, Ghana), Portugal (Max Plank Institute, Germany), Scott Weaver (UTMB USA) Pete Crompton (NIAID), we are undertaking a novel disease surveillance program by harnessing mosquitoes as samplers of pathogens from humans, domestic and especially wild hosts. This innovative project (funded in part by the Science for Africa Foundation and The Pandemic Science Institute, Oxford UK 2025—2030) will address regional and global vulnerability to epidemics. Due to its high biodiversity, Africa harbors many zoonotic pathogens of concern e.g., Ebola, Zika. Further, most African countries have limited capacity to sustain disease surveillance. Systematic surveillance of wild mammals and birds is especially lacking and knowledge on geographical distribution, natural/reservoir hosts, sylvatic vectors, etc. is poorly known. In this project, we focus on the “urban-rural-forest continuum” and describe the species compositions of mosquitoes, vertebrate hosts, and pathogens along it. Together we will assess connectivity across these environments in Mali, Ghana, and Burkina Faso. We analyze mosquito i) bloodmeals to identify the vertebrate host (e.g., human, chicken, bat) and its past exposure to pathogens using a multi-pathogen Luminex serological assay. The assays target antibodies to ≥10 pathogens with epidemic potential including Marburg, Lassa, Mpox, avian flu, Chikungunya, and dengue, ii) employ metagenomics to detect pathogens in mosquitoes; and iii) integrate information to guide public health decisions that protect local, regional, and global interests. Currently we carry out preliminary field operations while we develop SOPs to ensure high-quality comparable results across countries.