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. 2017 Jan 17;14(1):e1002213.
doi: 10.1371/journal.pmed.1002213. eCollection 2017 Jan.

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

Affiliations

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

Fernando Abad-Franch et al. PLoS Med. .

Abstract

Background: Mosquito-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 findings: We 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.

Conclusions: Mosquito-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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Study site: the city of Manacapuru, state of Amazonas, Brazil.
The black circles indicate the location of the 100 dwellings monitored for mosquito vectors; the green circles indicate the location of the 1,000 pyriproxyfen dissemination stations. Circles are overlaid on a schematic of Manacapuru; locations are approximate. The map of Latin America was drawn using the maps library in R 3.1.2 (https://www.r-project.org/).
Fig 2
Fig 2. Changes in mosquito population metrics following deployment of mosquito-disseminated pyriproxyfen: descriptive graphs.
(A) Monthly dwelling infestation by Aedes spp. (percent of dwellings in which at least one Ae. albopictus or Ae. aegypti juvenile was present in sentinel breeding sites [SBSs]); error bars are score 95% confidence intervals. (B) Mean monthly numbers of Aedes juveniles per SBS. (C) Monthly Aedes juvenile mortality (overall percent of juveniles that died before reaching adulthood); error bars are score 95% confidence intervals. (D) Mean monthly adult Aedes emergence (number of juvenile Aedes that developed into adults in each SBS); error bars are two standard errors. In all panels, the periods of citywide (dark grey) and focal (light grey) pyriproxyfen (PPF) dissemination are highlighted on the x-axes. Color coding in (A–C): red, pre-intervention (baseline) period, with orange indicating that just one survey was conducted in February 2015; dark green, citywide PPF dissemination; light green, focal PPF dissemination; blue, post-intervention period, with light blue indicating that just one survey was conducted in January 2016. Color coding in (D): red, females; blue, males; shaded area, total adult emergence; lighter red/blue, single-survey months (February 2015 and January 2016).
Fig 3
Fig 3. Monthly female Aedes albopictus emergence in each of the 100 surveillance dwellings.
The distribution of dwellings (black dots) and pyriproxyfen dissemination stations (green dots) is shown in the first panel, where dots are overlaid on a schematic of Manacapuru. In the remaining panels, bubble size is proportional to the number of emerging Ae. albopictus females; the scale is shown as a grey bubble in the second panel. For each month, the total number of emerging Ae. albopictus females is shown in the upper right corner of the panel. Color coding: brown, pre-intervention (baseline) period, with yellow indicating a single-survey month; dark green, citywide PPF dissemination; light green, focal PPF dissemination; blue, post-intervention period, with light blue indicating a single-survey month. Temporal boundaries between periods are highlighted by colored vertical bars.
Fig 4
Fig 4. Monthly female Aedes aegypti emergence in each of the 100 surveillance dwellings.
The distribution of dwellings (black dots) and pyriproxyfen dissemination stations (green dots) is shown in the first panel, where dots are overlaid on a schematic of Manacapuru. In the remaining panels, bubble size is proportional to the number of emerging Ae. aegypti females; the scale is shown as a grey bubble in the second panel. For each month, the total number of emerging Ae. aegypti females is shown in the upper right corner of the panel. Color coding: brown, pre-intervention (baseline) period, with yellow indicating a single-survey month; dark green, citywide PPF dissemination; light green, focal PPF dissemination; blue, post-intervention period, with light blue indicating a single-survey month. Temporal boundaries between periods are highlighted by colored vertical bars.
Fig 5
Fig 5. Estimated impact of mosquito-disseminated pyriproxyfen on Aedes populations: results of generalized linear mixed models.
(A) Mean monthly Aedes juvenile catch per dwelling: dots, observed values (in grey, values adjusted for single-survey months); solid line, model predictions (red, pre-intervention period; dark green, citywide pyriproxyfen [PPF] dissemination; light green, focal PPF dissemination; blue, post-intervention period); dotted line, model-predicted trajectory in the absence of intervention as a function of monthly rainfall and adjusted for the number of operational sentinel breeding sites and dwelling-level clustering. (B) Model-predicted percent change (with 95% confidence intervals) in juvenile mosquito catch relative to the pre-intervention period (CW, citywide PPF dissemination; F, focal dissemination; A, after PPF dissemination): diamonds, Ae. albopictus; triangles, Ae. aegypti; black circles, Aedes spp.; gold circles, all mosquito species. (C) Mean monthly Aedes adult emergence per dwelling, with coding as in (A). (D) Model-predicted percent change (with 95% confidence intervals) in adult Aedes emergence relative to the pre-intervention period, with periods coded as in (B); black circles, all Aedes adults; red circles, Aedes females; blue circles, Aedes males. In (A) and (C), the periods of citywide (dark grey) and focal (light grey) PPF dissemination are highlighted on the x-axes.
Fig 6
Fig 6. Monthly estimates of the basic reproductive number (R0) of mosquito-borne viruses similar to dengue, Zika, or chikungunya.
We considered scenarios ranging from optimistic to very adverse (see parameter values for each scenario in Table 1); the grey line corresponds to the worst-case scenario but with a higher value of the mean daily female mosquito death rate (μ = 0.3 instead of 0.1) to approximate data from wild Ae. aegypti populations (see [–37]). The pink dotted line shows empirical monthly values of the number of Aedes females per person (parameter m) in our study setting and period. The periods of citywide (dark grey) and focal (light grey) PPF dissemination are highlighted on the x-axis.

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