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. 2014 Sep 3:13:350.
doi: 10.1186/1475-2875-13-350.

Environmental temperatures significantly change the impact of insecticides measured using WHOPES protocols

Katey D Glunt  1 , Krijn P Paaijmans, Andrew F Read, Matthew B Thomas
Affiliations

Environmental temperatures significantly change the impact of insecticides measured using WHOPES protocols

Katey D Glunt et al. Malar J. .

Abstract

Background: Insecticides are critical components of malaria control programmes. In a variety of insect species, temperature plays a fundamental role in determining the outcome of insecticide exposure. However, surprisingly little is known about how temperature affects the efficacy of chemical interventions against malaria vectors.

Methods: Anopheles stephensi, with no recent history of insecticide exposure, were exposed to the organophosphate malathion or the pyrethroid permethrin at 12, 18, 22, or 26°C, using the WHO tube resistance-monitoring assay. To evaluate the effect of pre-exposure temperature on susceptibility, adult mosquitoes were kept at 18 or 26°C until just before exposure, and then moved to the opposite temperature. Twenty-four hours after exposure, mosquitoes exposed at <26°C were moved to 26°C and recovery was observed. Susceptibility was assessed in terms of survival 24 hours after exposure; data were analysed as generalized linear models using a binomial error distribution and logit link function.

Results: Lowering the exposure temperature from the laboratory standard 26°C can strongly reduce the susceptibility of female An. stephensi to the WHO resistance-discriminating concentration of malathion (χ2(df=3) = 29.0, p < 0.001). While the susceptibility of these mosquitoes to the resistance-discriminating concentration of permethrin was not as strongly temperature-dependent, recovery was observed in mosquitoes moved from 12, 18 or 22°C to 26°C 24 hours after exposure. For permethrin especially, the thermal history of the mosquito was important in determining the ultimate outcome of insecticide exposure for survival (permethrin: pre-exposure temperature: F1,29 = 14.2, p < 0.001; exposure temp: F1,29 = 1.1, p = 0.3; concentration: F1,29 = 85.2, p < 0.001; exposure temp x conc: F1,29 = 5.8, p = 0.02). The effect of acclimation temperature on malathion susceptibility depended on the exposure temperature (exposure temp: F1,79 = 98.4, p < 0.001; pre-exposure temp: F1,79 = 0.03, p = 0.9; pre-exp temp x exp temp F1,79 = 6.0, p = 0.02).

Conclusions: A single population of An. stephensi could be classified by WHO criteria as susceptible or resistant to a given chemical, depending on the temperature at which the mosquitoes were exposed. Investigating the performance of vector control tools under different temperature conditions will augment the ability to better understand the epidemiological significance of insecticide resistance and select the most effective products for a given environment.

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Figures

Figure 1
Figure 1
Annual temperature profiles at five meteorological-stations in Kenya, 2011. Solid circles indicate daily minimum temperatures and open circles indicate daily maximum temperatures. These locations, arranged top-to-bottom from lowest to highest altitude, are presented regardless of malaria transmission levels (Mombasa [9], Lodwar [10], Garissa [11], Nairobi [12], Kitale [13]), as a sample of the diversity of local temperature conditions. The WHO recommends that insecticide resistance testing be conducted at 25°C [6], indicated by the solid red line (previously, 27°C [5]; dashed line). Data obtained from NOAA, http://www.ncdc.noaa.gov/cdo-web.
Figure 2
Figure 2
Temperature history profiles of mosquitoes exposed to A) malathion or B) permethrin. All adults were reared under standard 26°C conditions. Up to one hour prior to exposure, females in each treatment group were moved to their exposure temperatures to adjust to the holding tubes; they remained at these temperatures throughout and after their hour-long insecticide exposure. After 24 hours at their treatment temperature, mosquitoes exposed to permethrin were moved to 26°C for 15 minutes in order to assess recovery.
Figure 3
Figure 3
Temperature history profiles of mosquitoes allowed to acclimate to different temperatures before insecticide exposure. Larvae were reared under standard 26°C conditions. Within two days of pupation, a cohort of mosquitoes was divided in half and moved to cages at 18 or 26°C to acclimate to those temperatures for up to five days. Each half of the cohort was divided prior the insecticide exposure, to create four treatment groups based on acclimation and exposure temperatures. After being separated into WHO tubes, mosquitoes remained at exposure temperatures throughout and for 24 hours after their hour-long insecticide exposure. After 24 hours at their treatment temperature, mosquitoes exposed to permethrin were moved to 26°C for 15 minutes in order to assess recovery.
Figure 4
Figure 4
Effect of exposure temperature on susceptibility to malathion. Panels depict survival of female An. stephensi A) one hour and B) 24 hours after exposure to 0 or 5% malathion at different temperatures. The dashed line at 0.02 indicates the level of survival above which populations are classified as resistant by the WHO [6].
Figure 5
Figure 5
Effect of temperature history on susceptibility to malathion. Panels depict survival of female An. stephensi A) one hour and B) 24 hours after exposure. Error bars (±1 SE) are centred at the mean survival of each treatment group, at each concentration of malathion. To show the relationship between dose and temperature treatment, lines connect the responses of each treatment group across increasing concentrations.
Figure 6
Figure 6
Effect of exposure temperature on susceptibility to permethrin. Panels depict survival of female An. stephensi A) one hour and B) 24 hours after exposure to 0 or 0.75% permethrin at different temperatures (Mean +/-1SE). The dashed line at 0.02 indicates the level of survival above which populations are classified as resistant by the WHO [6].
Figure 7
Figure 7
Effect of temperature history on susceptibility to permethrin. Panels depict survival of female An. stephensi A) one hour and B) 24 hours after exposure. Error bars (+/-1SE) are centred at the mean survival of each treatment group, at each concentration. Lines connect separate groups of mosquitoes, exposed to increasing concentrations of permethrin, to show the relationship between dose and temperature treatment.
Figure 8
Figure 8
Recovery of females exposed to permethrin at temperatures lower than 26°C. Hatched bars reflect survival 24 hours after exposure to permethrin at A) 12, 18 or 22°C in exposure temperature experiments or B) 18°C in acclimation experiments, using scoring criteria described by the WHO resistance-monitoring assay. Solid bars show the proportion of females surviving by this same measure after those groups experienced 15 minutes at 26°C. The recovery of these females suggests that post-exposure temperature can influence insecticide susceptibility. The dashed line at 0.02 indicates the level of survival above which populations are classified as ‘resistant’ by the WHO.
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