By Justine Rouge,

Malaria is the most important human parasitic disease affecting human and whose the global burden is primarily supported by the Sub-Saharan African countries [1].

Vector control mainly using insecticide-treated nets (ITNs) and indoor residual spraying (IRS) remain the most effective ways to prevent malaria.

To date, the pyrethroids such as DDT* are the only one family of insecticides approved by the WHO for use in ITNs [1].

Nevertheless, the large use of insecticides over many years has selected several mechanisms of resistance to these ones [2], [3], which are now widespread among malaria vectors in Africa. (See the video below).

Source: Pyrethroid resistance trends in Anopheles. sp (irmapper.com)

Thus, it appears as a major threat to sustaining the efficacy of malaria control.

Therefore, it’s important to maintain insecticide monitoring at all time in order to follow the progress of insecticides resistance or susceptibility of mosquitoes.
Currently, alternative strategies in insecticide-based practices are studied for vector control.

The combination of pyrethroids with synergists restoring the insecticide susceptibility of resistant mosquitoes (ex: Piperonyl butoxide (PBO)) [4], [5], or with non-neurotoxic insecticide (ex: Chlorfenapyr), or with molecules affecting the offspring of female mosquitoes (ex: Pyriproxyfen) are the most advanced alternative strategies [6].

However, insecticide susceptibility status of vector populations evaluated under standard insectary test conditions can give a false picture of the threat, as the insecticide toxicity and therefore its efficacy not only depends on the active chemical ingredient but depends also on its formulation, the biology of the insect, and the thermal environment in which the insect and insecticide interact [7].

Indeed, it was shown that the environmental temperature is a critical factor influencing insecticides toxicity [7]–[9] and the relationship between insecticide-induced toxicity and temperature can be described in terms of temperature coefficient (TC) which will be positive if the insecticide is most effective at higher temperature or negative if the insecticide is more toxic at lower temperature.

Thus, different studies showed that temperature influences the insecticide efficacy against different malaria vector species with different levels of insecticide resistance such as Anopheles. gambiae and Anopheles. stephensi [9]–[11].

Despite these results, this type of environmental factor remains widely unconsidered.

Recently, researchers from the University of Barcelona (Spain) in collaboration with researchers from the University of Johannesburg (South-Africa) studied the effect of temperature on the toxicity of different insecticides against 2 other malaria vector species from southern-Africa: An arabiensis and An. funestus [12] whose the resistant strains first.

To do this, they evaluated the expression of resistance of these mosquitoes using susceptible and resistant mosquito strains to the pyrethroid deltamethrin (An. Arabiensis and An. funestus) or the carbamate bendiocarb (An. funestus only), that they exposed to these previous insecticides at different temperatures: 18, 25 or 30ºC. Moreover, they examined the ability of the pyrethroid synergist PBO to restore the susceptibility to pyrethroid in resistant mosquitoes at these same temperatures pre-exposing these latter to the PBO before the insecticide exposure.

The use of extreme temperature (18 and 30°C) allowed to reproduce the variations of temperature existing during one day and during seasons in Africa as well as the variations of temperature between the different African countries.

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The low-temperature treatment (18 °C), represents a possible average night-time temperature or the average daily African highland temperature, while the high-temperature treatment, (30 °C), might be expected closer to mid-day, or an average in some parts of sub-Saharan Africa during the summer [13].

Researchers observed that temperature affects differently the toxicity of the deltamethrin and the one of the bendiocarb.

Indeed, the deltamethrin doesn’t have displayed a systematic positive or negative TC and the effect of temperature on its toxicity depended on the mosquito strain.
Against resistant An. arabiensis strains and susceptible An. funestus strains,
this insecticide was more lethal at extreme temperatures than the standard insectary temperature. However, against susceptible An. arabiensis strains, the deltamethrin toxicity decreased with higher temperatures.

Similar bimodal change in pyrethroid toxicity with temperature was observed in An. stephensi when exposed to permethrin [9] and could be explained by the interaction of chemical toxicity and the mosquito behaviour (irritancy) causing by the influence of the different temperatures in the case of pyrethroid insecticides.

On the contrary, the bendiocarb displayed a positive TC becoming more toxic and therefore more effective with increasing temperature against An. funestus strains either susceptible or resistant.
Similar results were observed with the Chlorfenapyr, an insecticide showing a positive TC and killing a more susceptible strain of An. gambiae with higher temperature [11].

Moreover, the pre-exposure to the PBO restored the deltamethrin susceptibility and was not affected by the temperature suggesting that the action of PBO would be independent of climatic conditions, an important result given that the next generation of ITNs has received approval from the WHO to integrate PBO as a pyrethroid resistance countermeasure [14], [15].

However, maybe it would have been interesting to test if a pre-exposure to the S,S,S-tributyl phosphorotrithioate (DEF) before the carbamate-bendiocarb exposure of the resistant An. funestus strains in order to test if the temperature have an effect on the action of the DEF, another insecticide-synergist known to reduce the carbamate-resistance in other insect such as the German cockroach (Blatella. germanica) [16], [17].

In any case, these results show a drastic change in the insecticide susceptibility of mosquitoes over the different temperatures showing that temperature is a determining factor in the efficacy of vector control tools. 

As part of the monitoring of insecticide resistance, these results highlight the importance to perform efficacy tests with actual vector control products under real field-conditions in order to limit the impact of confounding factors (such as temperature) and to choose the best-suited vector control strategies to fight infectious disease like malaria. 

Thanks for reading!

And don’t forget: Fight Malaria!

Notes:

*DDT: Dichlorodiphenyltrichloroethane is a chemical compound, an organochlorine, originally developed as an insecticide. It belongs to the pyrethroid family.

Bibliography

[1] World Health Organisation, World Malaria Report 2017
[2] D. Martinez-Torres et al., “Molecular characterization of pyrethroid knockdown resistance (KDR) in the major malaria vector Anopheles gambiae s.s.,” Insect Mol. Biol., vol. 7, no. 2, pp. 179–184, May 1998.
[3] H. Ranson, B. Jensen, J. M. Vulule, X. Wang, J. Hemingway, and F. H. Collins, “Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids,” Insect Mol. Biol., vol. 9, no. 5, pp. 491–497, Oct. 2000.
[4] F. Darriet and F. Chandre, “Combining Piperonyl Butoxide and Dinotefuran Restores the Efficacy of Deltamethrin Mosquito Nets Against Resistant Anopheles gambiae (Diptera: Culicidae),” J. Med. Entomol., vol. 48, no. 4, pp. 952–955, 2011.
[5] T. S. Churcher, N. Lissenden, J. T. Griffin, E. Worrall, and H. Ranson, “The impact of pyrethroid resistance on the efficacy and effectiveness of bednets for malaria control in Africa,” Elife, vol. 5, no. AUGUST, pp. 1–26, 2016.
[6] World Health Organization, “Conditions for deployment of mosquito nets treated with a pyrethroid and piperonyl butoxide,” vol. 2017, no. December, 2017.
[7] T. Miller and M. Adams, “Mode of action of pyrethroids,” in Insecticide Mode of Action, editor Coats JR, Ed. Cambridge: Academic Press, 1982, pp. p3-27.
[8] K. D. Glunt, J. I. Blanford, and K. P. Paaijmans, “Chemicals, Climate, and Control: Increasing the Effectiveness of Malaria Vector Control Tools by Considering Relevant Temperatures,” PLoS Pathog., vol. 9, no. 10, pp. 1–5, 2013.
[9] M. H. Hodjati and C. F. Curtis, “Effects of permethrin at different temperatures on pyrethroid-resistant and susceptible strains of Anopheles,” Med. Vet. Entomol., vol. 13, no. 4, pp. 415–422, Nov. 1999.
[10] K. D. Glunt, K. P. Paaijmans, A. F. Read, and M. B. Thomas, “Environmental temperatures significantly change the impact of insecticides measured using WHOPES protocols,” Malar. J., vol. 13, no. 1, pp. 1–11, 2014.
[11] R. M. Oxborough et al., “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,” Malar. J., vol. 14, no. 1, pp. 1–11, 2015.
[12] K. D. Glunt, S. V Oliver, R. H. Hunt, and K. P. Paaijmans, “The impact of temperature on insecticide toxicity against the malaria vectors Anopheles arabiensis and Anopheles funestus,” Malar J, vol. 17, no. 17, 2018.
[13] K. P. Paaijmans, S. Blanford, A. S. Bell, J. I. Blanford, A. F. Read, and M. B. Thomas, “Influence of climate on malaria transmission depends on daily temperature variation,” Proc. Natl. Acad. Sci., vol. 107, no. 34, pp. 15135–15139, 2010.
[14] WHO. Recommended long-lasting insecticidal nets. Geneva: World Health Organization. 2016.
[15] C. Pennetier et al., “Efficacy of Olyset® Plus, a New Long-Lasting Insecticidal Net Incorporating Permethrin and Piperonil-Butoxide against Multi-Resistant Malaria Vectors,” PLoS One, vol. 8, no. 10, p. e75134, Oct. 2013.

[16]   A. Sanei Dehkordi et al., “Synergists action of piperonyl butoxide and S,S,S-tributyl phosphorotrithioate on toxicity of carbamate insecticides against Blattella germanica,” Asian Pac. J. Trop. Med., vol. 10, no. 10, pp. 981–986, 2017.
[17]    S. M. Valles and S. J. Yu, “Detection and Biochemical Characterization of Insecticide Resistance in the German Cockroach (Dictyoptera: Blattellidae),” J. Econ. Entomol., vol. 89, no. 1, pp. 21–26, Feb. 1996.

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