Background: Historically, mosquito control programs successfully helped contain malaria and yellow fever, but recent efforts have been unable to halt the spread of dengue, chikungunya, or Zika, all transmitted by Aedes mosquitoes. Using a dengue transmission model and results from indoor residual spraying (IRS) field experiments, we investigated how IRS-like campaign scenarios could effectively control dengue in an endemic setting.

Methods and findings: In our model, we found that high levels of household coverage (75% treated once per year), applied proactively before the typical dengue season could reduce symptomatic infections by 89.7% (median of 1000 simulations; interquartile range [IQR]:[83.0%, 94.8%]) in year one and 78.2% (IQR: [71.2%, 88.0%]) cumulatively over the first five years of an annual program. Lower coverage had correspondingly lower effectiveness, as did reactive campaigns. Though less effective than preventative campaigns, reactive and even post-epidemic interventions retain some effectiveness; these campaigns disrupt inter-seasonal transmission, highlighting an off-season control opportunity. Regardless, none of the campaign scenarios maintain their initial effectiveness beyond two seasons, instead stabilizing at much lower levels of benefit: in year 20, median effectiveness was only 27.3% (IQR: [-21.3%, 56.6%]). Furthermore, simply ceasing an initially successful program exposes a population with lowered herd immunity to the same historical threat, and we observed outbreaks more than four-fold larger than pre-intervention outbreaks. These results do not take into account evolving insecticide resistance, thus long-term effectiveness may be lower if new, efficacious insecticides are not developed.

Conclusions: Using a detailed agent-based dengue transmission model for Yucatán State, Mexico, we predict that high coverage indoor residual spraying (IRS) interventions can largely eliminate transmission for a few years, when applied a few months before the typical seasonal epidemic peak. However, vector control succeeds by preventing infections, which precludes natural immunization. Thus, as a population benefits from mosquito control, it gradually loses naturally acquired herd immunity, and the control effectiveness declines; this occurs across all of our modeled scenarios, and is consistent with other empirical work. Long term control that maintains early effectiveness would require some combination of increasing investment, complementary interventions such as vaccination, and control programs across a broad region to diminish risk of importation.

Figures

Fig 1. Seasonality of dengue in the state of Yucatán (a-b), reference campaign periods (c), and effect of campaign start date on IRS cumulative 10 year effectiveness, in combination with three additional sensitivity dimensions (d-f; see Fig K, panel g in S1 Text for efficacy sensitivity).
Effectiveness sensitivity plots have the reference scenario highlighted in yellow. (a) Observed and modeled average dengue cases in the state of Yucatán, 1995-2015. (b) Model seasonal components: extrinsic incubation period (EIP) and mosquito population size (M(t)) combine to drive basic reproductive number (R₀); R₀ = 1 (the epidemic threshold in a fully susceptible population, dotted green) provided for reference. (c) Reference insecticide-active periods for 90 day rollout campaigns with 90 days of IRS durability, from start (treatment of first house, left bar) to end (insecticide expiration from last house, arrowhead). (d-f) Sensitivity to IRS coverage, with 90-day campaigns, 90-day durability, 80% efficacy, and 75% coverage as the reference scenario. Each sub-plot shows a univariate sensitivity study of ten-year effectiveness by start date from that reference.

**Fig 2. Predicted overall effectiveness of IRS and population immunity over 20 years.**
(a) New IRS campaigns show initial high effectiveness that wanes over time even without the evolution of insecticide resistance in mosquitoes. (b) If campaigns that have been effective are abruptly stopped, or if, for example, mosquitoes were to suddenly evolve complete insecticide resistance (red), epidemics much larger than baseline would likely occur until the human population re-established a high level of immunity. (c) At baseline (dashed black), a consistent fraction of the population is expected to have some level of naturally acquired immunity (seroprevalence; see Fig H in S1 Text for detailed breakdown). Because IRS is effective in reducing dengue infections (solid black, grey), seroprevalence decreases over time, permitting somewhat larger epidemics, but still smaller than baseline. If IRS is stopped or abruptly loses efficacy (red), population immunity rapidly climbs in response to the resulting very large epidemics.

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Forecasting the effectiveness of indoor residual spraying for reducing dengue burden

Abstract

Conflict of interest statement

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