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The activity of the pyrrole insecticide chlorfenapyr in mosquito bioassay: towards a more rational testing and screening of non-neurotoxic insecticides for malaria vector control.

Oxborough RM, N'Guessan R, Jones R, Kitau J, Ngufor C, Malone D, Mosha FW, Rowland MW - Malar. J. (2015)

Bottom Line: The efficacy of WHO recommended cone, cylinder and tunnel tests was compared for pyrethroids and chlorfenapyr.The endogenous circadian activity rhythm of anophelines results in inactivity by day and raised metabolism and flight activity by night.A model which explains improved toxicity of chlorfenapyr ITN when tested at night, and during the day at higher ambient temperature, is that activation of chlorfenapyr and disruption of respiratory pathways is enhanced when the insect is more metabolically and behaviourally active.

View Article: PubMed Central - PubMed

Affiliation: Department of Disease Control, London School of Hygiene and Tropical Medicine, London, UK. oxandbull@hotmail.com.

ABSTRACT

Background: The rapid selection of pyrethroid resistance throughout sub-Saharan Africa is a serious threat to malaria vector control. Chlorfenapyr is a pyrrole insecticide which shows no cross resistance to insecticide classes normally used for vector control and is effective on mosquito nets under experimental hut conditions. Unlike neurotoxic insecticides, chlorfenapyr owes its toxicity to disruption of metabolic pathways in mitochondria that enable cellular respiration. A series of experiments explored whether standard World Health Organization (WHO) guidelines for evaluation of long-lasting insecticidal nets, developed through testing of pyrethroid insecticides, are suitable for evaluation of non-neurotoxic insecticides.

Methods: The efficacy of WHO recommended cone, cylinder and tunnel tests was compared for pyrethroids and chlorfenapyr. To establish bioassay exposure times predictive of insecticide-treated net (ITN) efficacy in experimental hut trials, standard three-minute bioassays of pyrethroid and chlorfenapyr ITNs were compared with longer exposures. Mosquito behaviour and response to chlorfenapyr ITN in bioassays conducted at night were compared to day and across a range of temperatures representative of highland and lowland transmission.

Results: Standard three-minute bioassay of chlorfenapyr produced extremely low levels of mortality compared to pyrethroids. Thirty-minute day-time bioassay produced mortality closer to hut efficacy of chlorfenapyr ITN but still fell short of the WHO threshold. Overnight tunnel test with chlorfenapyr produced 100% mortality and exceeded the WHO threshold of 80%. The endogenous circadian activity rhythm of anophelines results in inactivity by day and raised metabolism and flight activity by night. A model which explains improved toxicity of chlorfenapyr ITN when tested at night, and during the day at higher ambient temperature, is that activation of chlorfenapyr and disruption of respiratory pathways is enhanced when the insect is more metabolically and behaviourally active.

Conclusions: Testing according to current WHO guidelines is not suitable for certain types of non-neurotoxic insecticide which, although highly effective in field trials, would be overlooked at the screening stage of evaluation through bioassay. Testing methods must be tailored to the characteristics and mode of action of each insecticide class. The WHO tunnel test on night-active anophelines is the most reliable bioassay for identifying the toxicity of novel insecticides.

No MeSH data available.


Related in: MedlinePlus

Circadian flight activity of inseminated non blood-fedAnopheles stephensiin an acoustic actograph under a 12:12 hour light/dark regime (top) and on transfer from a light/dark 12:12 hour to a constant darkness regime (bottom). Dark bars on x-axis refer to periods of darkness, white bars to periods of light. Hourly flight activity is a score (out of 60) indicating the number of minutes per hour during which mosquitoes undertook flight.
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Fig3: Circadian flight activity of inseminated non blood-fedAnopheles stephensiin an acoustic actograph under a 12:12 hour light/dark regime (top) and on transfer from a light/dark 12:12 hour to a constant darkness regime (bottom). Dark bars on x-axis refer to periods of darkness, white bars to periods of light. Hourly flight activity is a score (out of 60) indicating the number of minutes per hour during which mosquitoes undertook flight.

Mentions: While An. gambiae responded to the toxic action of pyrethroid exposure by day and night, response to chlorfenapyr exposure was more evident in the night-time assay (tunnel test) than in the day-time assays (cone and cylinder). To explore this further the resting and flight activity of mosquitoes in chambers of similar size to cones was examined using an actograph to record spontaneous flight activity. In the LD 12:12 regime, sugar-fed inseminated females showed no activity during the 12-hour light phase but during the dark phase there was an activity peak shortly after light off, followed by short bursts of intermittent activity throughout the 12 hours of darkness and a small activity peak at ‘dawn’ as the dimmer switched from darkness to light (Figure 3). When, in the next experiment, the LD 12:12 regime was changed to constant darkness (DD 12:12), a peak of flight activity occurred regularly at 24-hour intervals during the period which coincided with the former dark phase but not the former light phase (Figure 3). Thus the activity observed in the dark phase of LD 12:12 was not a response to the switch from light to dark but the expression of a free-running circadian activity rhythm with a 24-hour periodicity that was being expressed during the dark phase of LD 12:12 cycles.Figure 3


The activity of the pyrrole insecticide chlorfenapyr in mosquito bioassay: towards a more rational testing and screening of non-neurotoxic insecticides for malaria vector control.

Oxborough RM, N'Guessan R, Jones R, Kitau J, Ngufor C, Malone D, Mosha FW, Rowland MW - Malar. J. (2015)

Circadian flight activity of inseminated non blood-fedAnopheles stephensiin an acoustic actograph under a 12:12 hour light/dark regime (top) and on transfer from a light/dark 12:12 hour to a constant darkness regime (bottom). Dark bars on x-axis refer to periods of darkness, white bars to periods of light. Hourly flight activity is a score (out of 60) indicating the number of minutes per hour during which mosquitoes undertook flight.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4390098&req=5

Fig3: Circadian flight activity of inseminated non blood-fedAnopheles stephensiin an acoustic actograph under a 12:12 hour light/dark regime (top) and on transfer from a light/dark 12:12 hour to a constant darkness regime (bottom). Dark bars on x-axis refer to periods of darkness, white bars to periods of light. Hourly flight activity is a score (out of 60) indicating the number of minutes per hour during which mosquitoes undertook flight.
Mentions: While An. gambiae responded to the toxic action of pyrethroid exposure by day and night, response to chlorfenapyr exposure was more evident in the night-time assay (tunnel test) than in the day-time assays (cone and cylinder). To explore this further the resting and flight activity of mosquitoes in chambers of similar size to cones was examined using an actograph to record spontaneous flight activity. In the LD 12:12 regime, sugar-fed inseminated females showed no activity during the 12-hour light phase but during the dark phase there was an activity peak shortly after light off, followed by short bursts of intermittent activity throughout the 12 hours of darkness and a small activity peak at ‘dawn’ as the dimmer switched from darkness to light (Figure 3). When, in the next experiment, the LD 12:12 regime was changed to constant darkness (DD 12:12), a peak of flight activity occurred regularly at 24-hour intervals during the period which coincided with the former dark phase but not the former light phase (Figure 3). Thus the activity observed in the dark phase of LD 12:12 was not a response to the switch from light to dark but the expression of a free-running circadian activity rhythm with a 24-hour periodicity that was being expressed during the dark phase of LD 12:12 cycles.Figure 3

Bottom Line: The efficacy of WHO recommended cone, cylinder and tunnel tests was compared for pyrethroids and chlorfenapyr.The endogenous circadian activity rhythm of anophelines results in inactivity by day and raised metabolism and flight activity by night.A model which explains improved toxicity of chlorfenapyr ITN when tested at night, and during the day at higher ambient temperature, is that activation of chlorfenapyr and disruption of respiratory pathways is enhanced when the insect is more metabolically and behaviourally active.

View Article: PubMed Central - PubMed

Affiliation: Department of Disease Control, London School of Hygiene and Tropical Medicine, London, UK. oxandbull@hotmail.com.

ABSTRACT

Background: The rapid selection of pyrethroid resistance throughout sub-Saharan Africa is a serious threat to malaria vector control. Chlorfenapyr is a pyrrole insecticide which shows no cross resistance to insecticide classes normally used for vector control and is effective on mosquito nets under experimental hut conditions. Unlike neurotoxic insecticides, chlorfenapyr owes its toxicity to disruption of metabolic pathways in mitochondria that enable cellular respiration. A series of experiments explored whether standard World Health Organization (WHO) guidelines for evaluation of long-lasting insecticidal nets, developed through testing of pyrethroid insecticides, are suitable for evaluation of non-neurotoxic insecticides.

Methods: The efficacy of WHO recommended cone, cylinder and tunnel tests was compared for pyrethroids and chlorfenapyr. To establish bioassay exposure times predictive of insecticide-treated net (ITN) efficacy in experimental hut trials, standard three-minute bioassays of pyrethroid and chlorfenapyr ITNs were compared with longer exposures. Mosquito behaviour and response to chlorfenapyr ITN in bioassays conducted at night were compared to day and across a range of temperatures representative of highland and lowland transmission.

Results: Standard three-minute bioassay of chlorfenapyr produced extremely low levels of mortality compared to pyrethroids. Thirty-minute day-time bioassay produced mortality closer to hut efficacy of chlorfenapyr ITN but still fell short of the WHO threshold. Overnight tunnel test with chlorfenapyr produced 100% mortality and exceeded the WHO threshold of 80%. The endogenous circadian activity rhythm of anophelines results in inactivity by day and raised metabolism and flight activity by night. A model which explains improved toxicity of chlorfenapyr ITN when tested at night, and during the day at higher ambient temperature, is that activation of chlorfenapyr and disruption of respiratory pathways is enhanced when the insect is more metabolically and behaviourally active.

Conclusions: Testing according to current WHO guidelines is not suitable for certain types of non-neurotoxic insecticide which, although highly effective in field trials, would be overlooked at the screening stage of evaluation through bioassay. Testing methods must be tailored to the characteristics and mode of action of each insecticide class. The WHO tunnel test on night-active anophelines is the most reliable bioassay for identifying the toxicity of novel insecticides.

No MeSH data available.


Related in: MedlinePlus