Research Article: Mosquito-Disseminated Insecticide for Citywide Vector Control and Its Potential to Block Arbovirus Epidemics: Entomological Observations and Modeling Results from Amazonian Brazil

Date Published: January 17, 2017

Publisher: Public Library of Science

Author(s): Fernando Abad-Franch, Elvira Zamora-Perea, Sérgio L. B. Luz, Lorenz von Seidlein

Abstract: BackgroundMosquito-borne viruses threaten public health worldwide. When the ratio of competent vectors to susceptible humans is low enough, the virus’s basic reproductive number (R0) falls below 1.0 (each case generating, on average, <1.0 additional case) and the infection fades out from the population. Conventional mosquito control tactics, however, seldom yield R0 < 1.0. A promising alternative uses mosquitoes to disseminate a potent growth-regulator larvicide, pyriproxyfen (PPF), to aquatic larval habitats; this kills most mosquito juveniles and substantially reduces adult mosquito emergence. We tested mosquito-disseminated PPF in Manacapuru, a 60,000-inhabitant city (~650 ha) in Amazonian Brazil.Methods and FindingsWe sampled juvenile mosquitoes monthly in 100 dwellings over four periods in February 2014–January 2016: 12 baseline months, 5 mo of citywide PPF dissemination, 3 mo of focal PPF dissemination around Aedes-infested dwellings, and 3 mo after dissemination ended. We caught 19,434 juvenile mosquitoes (66% Aedes albopictus, 28% Ae. aegypti) in 8,271 trap-months. Using generalized linear mixed models, we estimated intervention effects on juvenile catch and adult emergence while adjusting for dwelling-level clustering, unequal sampling effort, and weather-related confounders. Following PPF dissemination, Aedes juvenile catch decreased by 79%–92% and juvenile mortality increased from 2%–7% to 80%–90%. Mean adult Aedes emergence fell from 1,077 per month (range 653–1,635) at baseline to 50.4 per month during PPF dissemination (range 2–117). Female Aedes emergence dropped by 96%–98%, such that the number of females emerging per person decreased to 0.06 females per person-month (range 0.002–0.129). Deterministic models predict, under plausible biological-epidemiological scenarios, that the R0 of typical Aedes-borne viruses would fall from 3–45 at baseline to 0.004–0.06 during PPF dissemination. The main limitations of our study were that it was a before–after trial lacking truly independent replicates and that we did not measure mosquito-borne virus transmission empirically.ConclusionsMosquito-disseminated PPF has potential to block mosquito-borne virus transmission citywide, even under adverse scenarios. Our results signal new avenues for mosquito-borne disease prevention, likely including the effective control of Aedes-borne dengue, Zika, and chikungunya epidemics. Cluster-randomized controlled trials will help determine whether mosquito-disseminated PPF can, as our findings suggest, develop into a major tool for improving global public health.

Partial Text: Fast global spread of mosquito-borne viruses is among the most pressing contemporary public health challenges [1,2]. The dengue, West Nile, and Japanese encephalitis viruses are well-known mosquito-transmitted pathogens, but we are currently witnessing the emergence of novel threats including chikungunya and Zika [1–6]. Both African in origin, these two viruses are causing large epidemics in the Americas and more restricted outbreaks in Europe, Southeast Asia, and the Pacific [5–7]. Ongoing Zika epidemics are particularly worrying because infection with this virus can cause Guillain-Barré syndrome and congenital central nervous system malformations including microcephaly [6–13].

This project was led by the Fundação Oswaldo Cruz (Brazilian Ministry of Health) in a joint initiative with local state and municipal health departments. Formal approval was not required for urban mosquito collection.

In this study we have shown that a sharp citywide decrease in mosquito vector populations followed the application of a low-technology tactic based on mosquito-disseminated PPF in a tropical town. Population declines were observed for Aedes and Culex spp., two foremost vectors of human disease, and for Limatus spp. The 95%–96% reduction in Aedes female emergence we report has the potential of blocking arbovirus transmission under scenarios ranging from somewhat optimistic to overtly adverse. The control of urban Culex spp. could have similar effects on the spread of important pathogens ranging from West Nile virus to lymphatic filariae; Culex spp. might in addition transmit Zika virus [38], although this is yet to be confirmed. Suppression of urban Limatus populations has less clear public health implications, but several bunyaviruses capable of infecting mammals have been isolated from mosquitoes of this day-biting genus in Amazonia [39].



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