The mode of action of spatial repellents and their impact on vectorial capacity of Anopheles gambiae sensu stricto

Sheila B Ogoma, Hassan Ngonyani, Emmanuel T Simfukwe, Antony Mseka, Jason Moore, Marta F Maia, Sarah J Moore, Lena M Lorenz, Sheila B Ogoma, Hassan Ngonyani, Emmanuel T Simfukwe, Antony Mseka, Jason Moore, Marta F Maia, Sarah J Moore, Lena M Lorenz

Abstract

Malaria vector control relies on toxicity of insecticides used in long lasting insecticide treated nets and indoor residual spraying. This is despite evidence that sub-lethal insecticides reduce human-vector contact and malaria transmission. The impact of sub-lethal insecticides on host seeking and blood feeding of mosquitoes was measured. Taxis boxes distinguished between repellency and attraction inhibition of mosquitoes by measuring response of mosquitoes towards or away from Transfluthrin coils and humans. Protective effective distance of coils and long-term effects on blood feeding were measured in the semi-field tunnel and in a Peet Grady chamber. Laboratory reared pyrethroid susceptible Anopheles gambiae sensu stricto mosquitoes were used. In the taxis boxes, a higher proportion of mosquitoes (67%-82%) were activated and flew towards the human in the presence of Transfluthrin coils. Coils did not hinder attraction of mosquitoes to the human. In the semi-field Tunnel, coils placed 0.3 m from the human reduced feeding by 86% (95% CI [0.66; 0.95]) when used as a "bubble" compared to 65% (95% CI [0.51; 0.76]) when used as a "point source". Mosquitoes exposed to coils inside a Peet Grady chamber were delayed from feeding normally for 12 hours but there was no effect on free flying and caged mosquitoes exposed in the semi-field tunnel. These findings indicate that airborne pyrethroids minimize human-vector contact through reduced and delayed blood feeding. This information is useful for the development of target product profiles of spatial repellent products that can be used to complement mainstream malaria vector control tools.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Taxis boxes experimental design.
Figure 1. Taxis boxes experimental design.
Two taxis boxes placed 1 m away from the stimulus/treatment that is: a human or human and a coil. Mosquitoes were introduced in the middle chamber of each taxis box and the stimulus/treatment was changed each day to determine the effect on orientation of mosquitoes.
Figure 2. Point source experimental set up.
Figure 2. Point source experimental set up.
These experiments were conducted in the semi – field tunnel. In the control, two coils were placed on one side of the human. The distance between the coils and the human was changed each day to determine the protective distance of coils. Coils were not used in the control. Mosquitoes were released inside the tunnel and they were left to acclimatize for 10 minutes and then the human started collecting mosquitoes that landed on the bare feet.
Figure 3. Bubble experimental set up.
Figure 3. Bubble experimental set up.
Experiments were conducted in the semi – field tunnel. A coil was placed equidistant on either side of the human. The distance was changed each night to determine the protective distance. Coils were not used in the control. Mosquitoes were released inside the tunnel and left to acclimatize for 10 minutes and then the human started collecting mosquitoes.
Figure 4. Dose response of mosquitoes to…
Figure 4. Dose response of mosquitoes to Transfluthrin coils with a human using taxis boxes.
Horizontal histogram presenting the percentage proportion of mosquitoes activated, attracted and repelled by control (no stimulus) and treatments: human alone, human + blank coil, human +0.015% Transfluthrin coil, human +0.030% Transfluthrin coil, human +0.045% Transfluthrin coil) in the taxis boxes. The table includes percentage proportions and their confidence intervals.
Figure 5. The effect of Transfluthrin coils…
Figure 5. The effect of Transfluthrin coils on blood feeding behavior of mosquitoes in a Peet Grady chamber.
Mosquitoes were exposed to different doses of Transfluthrin coils inside a Peet Grady chamber and later offered blood meals at different time intervals. The proportion of blood fed mosquitoes was compared between different doses and the control that had no coil. The proportion of blood fed mosquitoes was significantly lower than the control in all treatments after 25 minutes (a) and 1 hour (a). At 12 hours only 0.03% Transfluthrin coils significantly (b) reduced feeding compared to the control while after 24 hours there was no significant difference between all treatments and controls (c).
Figure 6. The effect of Transfluthrin coils…
Figure 6. The effect of Transfluthrin coils on blood feeding behavior of mosquitoes in a Semi-Field Tunnel.
The proportion of blood fed mosquitoes after they had been exposed to mosquito coils in the semi-field tunnel is presented in the two graphs. The graph on the left indicates caged mosquitoes and the one on the right indicates free flying mosquitoes. In the left graph the proportion of blood fed mosquitoes was significantly lower in the treatment compared to the control after only after 1 hour. In the right graph, the proportion of blood fed mosquitoes was not significantly different between controls and treatments at all times.

References

    1. Garrett-Jones C (1964) The human blood index of malarial vectors in relationship to epidemiological assessment. Bull Wld Hlth Org 30:241–261.
    1. Koella JC (1991) On the use of mathematical models of malaria transmission. Acta Tropica 49:1–25.
    1. Kiszewski AE, Mellinger A, Spielman A, Malaney P, Sachs SE, et al. (2004) A global index representing the stability of malaria transmission. American Journal of Tropical Medicine and Hygiene 70:486–498.
    1. Takken W, Knols BG (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44:131–157.
    1. Gillies MT, Wilkes TJ (1970) The range of attraction of single baits for some West African mosquitoes. Bull Entomol Res 60:225–235.
    1. Gillies MT, Wilkes TJ (1972) The range of attraction of animal baits and carbon dioxide for mosquitoes. Studies in a freshwater area of West Africa. Bull Entomol Res 61:389–404.
    1. Lorenz LM, Keane A, Moore JD, Munk CJ, Seeholzer L (2013) Taxis assays measure directional movement of mosquitoes to olfactory cues. Parasit Vectors 6:131.
    1. Van der Goes van Naters WM, Carlson JR (2006) Insects as chemosensors of humans and crops. Nature 444:302–307.
    1. Hallem EA, Nicole Fox A, Zwiebel LJ, Carlson JR (2004) Olfaction: mosquito receptor for human-sweat odorant. Nature 427:212–213.
    1. Leal WS (2013) Odorant Reception in Insects: Roles of Receptors, Binding Proteins, and Degrading Enzymes. Annu Rev Entomol 58:373–391.
    1. Cook SA, Khan ZR, Pickett JA (2007) The Use of Push-Pull Strategies in Integrated Pest Management. Annu Rev Entomol 52:375–400.
    1. Mita T, Kaneko A, Lum JK, Bwijo B, Takechi M, et al. (2003) Recovery of chloroquine sensitivity and low prevalence of the Plasmodium falciparum chloroquine resistance transporter gene mutation K76T following the discontinuance of chloroquine use in Malawi. Am J Trop Med Hyg 68:413–415.
    1. della Torre A, Merzagora L, Powell JR, Coluzzi M (1997) Selective introgression of paracentric inversions between two sibling species of the Anopheles gambiae complex. Genetics 146:239–244.
    1. Knols BG, Willemse L, Flint S, Mate A (1993) A trial to control the tsetse fly, Glossina morsitans centralis, with low densities of odour-baited targets in west Zambia. Med Vet Entomol 7:161–169.
    1. Williams CR, Long SA, Russell RC, Ritchie SA (2006) Field efficacy of the BG- Sentinel compared with CDC backpack aspirators and CO2 baited EVS traps for collection of adult Aedes aegypti in Cairns, Queensland, Australia. J Am Mosq Contr Assoc 22:296–300.
    1. Govella NJ, Okumu FO, Killeen GF (2010) Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg 82:415–419.
    1. Kitau J, Pates H, Rwegoshora TR, Rwegoshora D, Matowo J, et al. (2010) The effect of Mosquito Magnet Liberty Plus trap on the human mosquito biting rate under semi-field conditions. J Am Mosq Control Assoc 26:287–294.
    1. Hill N, Lenglet A, Arnéz AM, Carneiro I (2007) Plant based insect repellent and insecticide treated bed nets to protect against malaria in areas of early evening biting vectors: double blind randomised placebo controlled clinical trial in the Bolivian Amazon. BMJ 335:1001–1002.
    1. Kennedy JS (1947) The excitant and repellent effects on mosquitoes of sublethal contacts with DDT. Bull Entomol Res 37:593–607.
    1. Dethier GV, Browne BL, Smith NC (1960) The designation of chemicals in terms of the responses they elicit from insects. J Econ Ento 53:134–136.
    1. Bernier UR, Kline DL, Posey KH (2007) Human emanations and related Natural Compounds That Inhibit Mosquito Host-Finding Abilities. Insect Repellents Principles, Methods and Uses: Taylor and Francis Group. pp.77–100.
    1. Bohbot JD, Dickens JD (2010) Insect repellents: modulators of mosquito odorant receptor activity. PLoS One 5.
    1. Dogan EB, Rossignol PA (1999) An olfactometer for discriminating between attraction, inhibition, and repellency in mosquitoes (Diptera: Culicidae). J Med Entomol 36:788–793.
    1. Lucas JR, Shono Y, Iwasaki T, Ishiwatari T, Spero N, et al. (2007) U.S. Laboratories and field trials of metofluthrin (SumiOne) emanators for reducing mosquito biting outdoors. Journal of the American Mosquito Control Association 23:47–54.
    1. Ogoma SB, Moore SJ, Maia MF (2012) A systematic review of mosquito coils and passive emanators: defining recommendations for spatial repellency testing methodologies. Parasit Vectors
    1. Chavasse DC (1996) The relationship between mosquito density and mosquito coil sales in Dar es Salaam. Trans R Soc Trop Med Hyg 90:493.
    1. Ogoma BS, Moore SJ, Maia MF (2012) A systematic review of mosquito coils and passive emanators: defining recommenations for spatial repellency testing methodologies. Parasites & vectors 5:287.
    1. Ogoma BS, Lorenz LM, Ngonyani H, Sangusangu R, Kitumbukile M, et al. (2014) An experimental hut study to quantify the effect of DDT and airborne pyrethroids on entomological parameters of malaria transmission. Malar J 13:131.
    1. Bernier R, Kline DL, Posey KH (2006) Human Emanations and Related Natural Compounds That Inhibit Mosquito Host-Finding Abilities. In: Debboun M, Frances SP, Strickman AD, editors. Insect Repellents: Principles, Methods, and Uses. pp.77–100.
    1. WHOPES (2009) Guidelines for efficacy testing of mosquito repellents for human skin Geneva: World Health Organisation.
    1. R Development Core Team (2011) Foundation for Statistical Computing Vienna. Retrieved 2011 fhwR-po. R: A language and environment for statistical computing. R In: Team RDC, editor.
    1. Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0999375-39 Retrieved 2011. Available: .
    1. Kline DL, Bernier UR, Posey KH, Barnard DR (2003) Olfactometric evaluation of spatial repellents for Aedes aegypti. J Med Entomol 40:463–467.
    1. Winney R (1975) Pyrethrins and pyrethroids in coils- a review. Pyreth Post 13:17–22.
    1. Chadwick PR (1975) The activity of some pyrethroids, DDT and lindane in smoke from coils for biting inhibition, knock down and kill of mosquitoes (Diptera, Culicidae). Bull Ento Res 67:97–101.
    1. Obermayr U, Ruther J, Bernier U, Rose A, Geier M (2012) Laboratory Evaluation Techniques to Investigate the Spatial Potential of Repellents for Push and Pull Mosquito Control Systems. J Med Entomol 49:1387–1397.
    1. Bernier UR, Furman KD, Kline DL, Allan SA, Barnard DR (2005) Comparison of contact and spatial repellency of catnip oil and N, N-diethyl-3-methylbenzamide (Deet) against mosquitoes. J Med Entomol 42:306–311.
    1. Bohbot JD, Fu L, Le TC, Chauhan K, Cantrell CL, et al. (2011) Multiple activities of insect repellents on odorant receptors in mosquitoes. Medical and Veterinary Entomology 25:436–444.
    1. Dickens JC, Bohbot JD (2013) Mini review: Mode of action of mosquito repellents Pesticide Biochemistry and Physiology.
    1. Miller JE, Gibson G (1994) Behavioral Response of Host-Seeking Mosquitoes (Diptera: Culicidae) to Insecticide-Impregnated Bed Netting: A New Approach to Insecticide Bioassays. J Med Entomol 31:114–122.
    1. Maia MF, Onyango SP, Thele M, Simfukwe ET, Turner EL, et al. (2013) Do Topical Repellents Divert Mosquitoes within a Community? - Health Equity Implications of Topical Repellents as a Mosquito Bite Prevention Tool. PLoS One 8:e84875.
    1. Cohnstaedt LW, Allan SA (2011) Effects of sublethal pyrethroid exposre on host-seeking behaviour of female mosquitoes. J Vec Ecol 36:395–403.
    1. Read AF, Penelope AL, Thomas MB (2009) How to make evoluntion-proof insecticides for malaria control. PLoS Biol 7:e1000058.
    1. Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, et al. (2010) Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9:62.
    1. Bugoro H, Iro'ofa C, Mackenzie DO, Apairamo A, Hevalao W, et al. (2011) Changes in vector species composition and current vector biology and behaviour will favour malaria elimination in Santa Isabel Province, Solomon Islands. Malar J 10:287.
    1. Durnez L, Coosemans M (2013) Anopheles mosquitoes - New insights into malaria vectors. Residual transmission of malaria: an old issue for new approaches: 671–704.

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera