Undesirable consequences of insecticide resistance following Aedes aegypti control activities due to a dengue outbreak

Abstract

Background: During a dengue outbreak with co-circulation of DENV-1 and -2 in the city of Boa Vista, one patient was diagnosed with DENV-4, a serotype supposed absent from Brazil for almost 30 years. The re-emergence of DENV-4 triggered the intensification of mechanical and chemical Aedes aegypti control activities in order to reduce vector density and avoid DENV-4 dissemination throughout the country.

Methods/principal findings: Vector control activities consisted of (a) source reduction, (b) application of diflubenzuron against larvae and (c) vehicle-mounted space spraying of 2% deltamethrin to eliminate adults. Control activity efficacy was monitored by comparing the infestation levels and the number of eggs collected in ovitraps before and after interventions, performed in 22 Boa Vista districts, covering an area of ∼ 80% of the city and encompassing 56,837 dwellings. A total of 94,325 containers were eliminated or treated with diflubenzuron. The most frequently positive containers were small miscellaneous receptacles, which corresponded to 59% of all positive breeding sites. Insecticide resistance to deltamethrin was assessed before, during and after interventions by dose-response bioassays adopting WHO-based protocols. The intense use of the pyrethroid increased fourfold the resistance ratio of the local Ae. aegypti population only six months after the beginning of vector control. Curiously, this trend was also observed in the districts in which no deltamethrin was applied by the public health services. On the other hand, changes in the resistance ratio to the organophosphate temephos seemed less influenced by insecticide in Boa Vista.

Conclusions: Despite the intense effort, mosquito infestation levels were only slightly reduced. Besides, the median number of eggs in ovitraps remained unaltered after control activity intensification. The great and rapid increase in pyrethroid resistance levels of natural Ae. aegypti populations is discussed in the context of both public and domestic intensification of chemical control due to a dengue outbreak.

Figure 1. Timeline of vector control activities related to DENV-4 confirmation in Boa Vista, Roraima State.

Intensification of vector source reduction activities started at the 32^nd epidemiological week ('during').

Figure 2. Schematic view of Boa Vista city.

Districts in dark grey belong to Zone 1 and were exposed to an intense vector control, which included source reduction, diflubenzuron application against larvae and six cycles of deltamethrin applied on a vehicle-mounted basis to reduce adult mosquito density. Light grey shows Zone 2, where source reduction and diflubenzuron also took place, but only three cycles of deltamethrin were applied. Finally, Zone-3 represents all the districts that had no intervention, i.e., vectorial control was routinely performed. Insecticide resistance evaluations were performed with two groups of pooled samples: those derived from all districts of Zone 1 and, for Zone 3, material collected at districts labeled with an asterisk.

Figure 3. Percentage of houses harboring Ae. aegypti immature forms (HI) in Boa Vista between Jan/2008 and Oct/2010.

Zones 1–3 are shown in Figure 2.

Figure 4. Median, 25 and 75 percentiles for the quantitative series of eggs collected in ovitraps in (A) Zone 1, (B) Zone 2 and (C) Zone 3.

The dashed line refers to the intervention, and the number of eggs per ovitrap per week was assessed before (five weeks prior) and after (five weeks later) the intensification of control activities.