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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

‘Repel all biters’: an enhanced collection of endophilic Anopheles gambiae and Anopheles arabiensis in CDC light-traps, from the Kagera Region of Tanzania, in the presence of a combination mosquito net impregnated with piperonyl butoxide and permethrin

Authors: Corey LeClair, Judith Cronery, Enock Kessy, Elsa V. E. Tomás, Yohannes Kulwa, Franklin W. Mosha, Mark Rowland, Natacha Protopopoff, J. Derek Charlwood

Published in: Malaria Journal | Issue 1/2017

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Abstract

Background

Mosquito nets containing synergists designed to overcome metabolic resistance mechanisms in vectors have been developed. These may enhance excitability in the mosquitoes and affect how they respond to CDC light-traps. Investigating the behaviour of vectors of disease in relation to novel mosquito nets is, therefore, essential for the design of sampling and surveillance systems.

Methods

In an initial experiment in Muleba, Tanzania, nine bedrooms from three housing clusters were sampled. CDC light-traps were operated indoors next to occupied untreated nets (UTN), Olyset® long lasting insecticidal net (LLIN) and Olyset Plus® LLIN containing piperonyl butoxide (PBO) synergist. Nets were rotated daily between the nine rooms over nine nights. A further series of experiments using the nets on alternate nights in a single room was undertaken during the short rains. Anopheles gambiae s.l. were collected in CDC light-traps, a window-trap and Furvela tent-trap. Anopheles gambiae s.l. were identified to species by polymerase chain reaction (PCR).

Results

In the initial experiment 97.7% of the 310 An. gambiae s.l. were An. gambiae s.s., the remainder being Anopheles arabiensis. The number of mosquitoes collected from 81 light-trap collections was greater in the presence of an Olyset [density rate ratio 1.81, 95% CI (1.22–2.67), p = 0.003] relative to an UTN. In a second experiment, in the wet season 84% of the 180 An. gambiae s.l. identified were An. arabiensis. The number of An. gambiae s.l. collected from a light-trap compared to a tent-trap was significantly higher when an Olyset Plus net was used compared to an UTN. Survival of the mosquitoes in the window trap was not reduced by the use of an Olyset Plus net in the bedroom relative to an Olyset net.

Conclusion

Mosquitoes entering bedrooms, even those susceptible to pyrethroids, were not killed by contact with an Olyset Plus LLIN. The enhanced numbers of An. gambiae or An. arabiensis collected in light-traps when a treated net is used requires further experimentation and may be because of a heightened escape reaction on the part of the mosquito.
Literature
1.
go back to reference Miller JE, Lindsay SW, Armstrong JRM. Experimental hut trials of bednets impregnated with synthetic pyrethroid or organophosphate insecticide for mosquito control in The Gambia. Med Vet Entomol. 1991;5:465–76.CrossRefPubMed Miller JE, Lindsay SW, Armstrong JRM. Experimental hut trials of bednets impregnated with synthetic pyrethroid or organophosphate insecticide for mosquito control in The Gambia. Med Vet Entomol. 1991;5:465–76.CrossRefPubMed
2.
go back to reference Lines JD, Myamba J, Curtis CF. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol. 1987;1:37–51.CrossRefPubMed Lines JD, Myamba J, Curtis CF. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol. 1987;1:37–51.CrossRefPubMed
3.
go back to reference Lindsay SW, Adiamah JH, Armstrong JRM. The effect of permethrin-impregnated bednets on house entry by mosquitoes (Diptera: Culicidae) in The Gambia. Bull Entomol Res. 1992;82:49–55.CrossRef Lindsay SW, Adiamah JH, Armstrong JRM. The effect of permethrin-impregnated bednets on house entry by mosquitoes (Diptera: Culicidae) in The Gambia. Bull Entomol Res. 1992;82:49–55.CrossRef
4.
go back to reference Smith Paintain L, Awini E, Addei S, Kukula V, Nikoi C, Sarpong D, et al. Evaluation of a universal long-lasting insecticidal net (LLIN) distribution campaign in Ghana: cost effectiveness of distribution and hang-up activities. Malar J. 2014;13:71.CrossRefPubMedPubMedCentral Smith Paintain L, Awini E, Addei S, Kukula V, Nikoi C, Sarpong D, et al. Evaluation of a universal long-lasting insecticidal net (LLIN) distribution campaign in Ghana: cost effectiveness of distribution and hang-up activities. Malar J. 2014;13:71.CrossRefPubMedPubMedCentral
5.
go back to reference Magbity EB, Lines JD, Marbiah MT, David K, Peterson E. How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets? Bull Entomol Res. 2002;92:71–6.CrossRefPubMed Magbity EB, Lines JD, Marbiah MT, David K, Peterson E. How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets? Bull Entomol Res. 2002;92:71–6.CrossRefPubMed
6.
go back to reference Fornadel CM, Norris LC, Norris DE. Centers for disease control light traps for monitoring Anopheles arabiensis human biting rates in an area with low vector density and high insecticide-treated bed net use. Am J Trop Med Hyg. 2010;83:838–42.CrossRefPubMedPubMedCentral Fornadel CM, Norris LC, Norris DE. Centers for disease control light traps for monitoring Anopheles arabiensis human biting rates in an area with low vector density and high insecticide-treated bed net use. Am J Trop Med Hyg. 2010;83:838–42.CrossRefPubMedPubMedCentral
7.
go back to reference Kirby MJ, Green C, Milligan PM, Sismanidis C, Jasseh M, Conway DJ, et al. Risk factors for house-entry by malaria vectors in a rural town and satellite villages in The Gambia. Malar J. 2008;7:2.CrossRefPubMedPubMedCentral Kirby MJ, Green C, Milligan PM, Sismanidis C, Jasseh M, Conway DJ, et al. Risk factors for house-entry by malaria vectors in a rural town and satellite villages in The Gambia. Malar J. 2008;7:2.CrossRefPubMedPubMedCentral
8.
go back to reference Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, et al. Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae. Med Vet Entomol. 2000;14:81–8.CrossRefPubMed Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, et al. Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae. Med Vet Entomol. 2000;14:81–8.CrossRefPubMed
9.
go back to reference Kawada H, Ohashi K, Dida GO, Sonye G, Njenga SM, Mwandawiro C, et al. Insecticidal and repellent activities of pyrethroids to the three major pyrethroid-resistant malaria vectors in western Kenya. Parasit Vectors. 2014;7:208.CrossRefPubMedPubMedCentral Kawada H, Ohashi K, Dida GO, Sonye G, Njenga SM, Mwandawiro C, et al. Insecticidal and repellent activities of pyrethroids to the three major pyrethroid-resistant malaria vectors in western Kenya. Parasit Vectors. 2014;7:208.CrossRefPubMedPubMedCentral
10.
go back to reference Agossa FR, Gnanguenon V, Anagonou R, Azondekon R, Aízoun N, Sovi A, et al. Impact of insecticide resistance on the effectiveness of pyrethroid-based malaria vectors control tools in Benin: decreased toxicity and repellent effect. PLoS ONE. 2015;10:e0145207.CrossRefPubMedPubMedCentral Agossa FR, Gnanguenon V, Anagonou R, Azondekon R, Aízoun N, Sovi A, et al. Impact of insecticide resistance on the effectiveness of pyrethroid-based malaria vectors control tools in Benin: decreased toxicity and repellent effect. PLoS ONE. 2015;10:e0145207.CrossRefPubMedPubMedCentral
11.
go back to reference Strode C, Donegan S, Garner P, Enayati AA, Hemingway J. The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis. PLoS Med. 2014;11:e1001619.CrossRefPubMedPubMedCentral Strode C, Donegan S, Garner P, Enayati AA, Hemingway J. The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis. PLoS Med. 2014;11:e1001619.CrossRefPubMedPubMedCentral
12.
go back to reference Hemingway J, Hawkes NJ, McCarroll L, Ranson H. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004;34:653–65.CrossRefPubMed Hemingway J, Hawkes NJ, McCarroll L, Ranson H. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004;34:653–65.CrossRefPubMed
13.
go back to reference West PA, Protopopoff N, Wright A, Kivaju Z, Tigererwa R, Mosha FW, et al. Indoor residual spraying in combination with insecticide-treated nets compared to insecticide-treated nets alone for protection against malaria: a cluster randomised trial in Tanzania. PLoS Med. 2014;11:e1001630.CrossRefPubMedPubMedCentral West PA, Protopopoff N, Wright A, Kivaju Z, Tigererwa R, Mosha FW, et al. Indoor residual spraying in combination with insecticide-treated nets compared to insecticide-treated nets alone for protection against malaria: a cluster randomised trial in Tanzania. PLoS Med. 2014;11:e1001630.CrossRefPubMedPubMedCentral
14.
go back to reference Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, et al. High level of resistance in the mosquito Anopheles gambiae to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013;12:149.CrossRefPubMedPubMedCentral Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, et al. High level of resistance in the mosquito Anopheles gambiae to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013;12:149.CrossRefPubMedPubMedCentral
15.
go back to reference WHOPES. Report of the fifteenth WHOPES working group meeting. Geneva: WHOPES; 2012. p. 108. WHOPES. Report of the fifteenth WHOPES working group meeting. Geneva: WHOPES; 2012. p. 108.
16.
go back to reference Lines JD, Curtis CF, Wilkes TJ, Njunwa KJ. Monitoring human-biting mosquitoes (Diptera: Culicidae) in Tanzania with light-traps hung beside mosquito nets. Bull Entomol Res. 1991;81:77–84.CrossRef Lines JD, Curtis CF, Wilkes TJ, Njunwa KJ. Monitoring human-biting mosquitoes (Diptera: Culicidae) in Tanzania with light-traps hung beside mosquito nets. Bull Entomol Res. 1991;81:77–84.CrossRef
17.
go back to reference Charlwood JD, LeClair C. The Furvela tent-trap Mk 1.1 for the collection of outdoor biting mosquitoes. Peer J. 2017. Charlwood JD, LeClair C. The Furvela tent-trap Mk 1.1 for the collection of outdoor biting mosquitoes. Peer J. 2017.
18.
go back to reference Gillies MT, De Meillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). Johannesburg: South African Institute for Medical Research; 1968. Gillies MT, De Meillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). Johannesburg: South African Institute for Medical Research; 1968.
19.
go back to reference Gillies Coetzee MMT. A supplement to the anophelinae of Africa south of the Sahara (Afrotropical Region). Johannesburg: South African Institute for Medical Research; 1987. Gillies Coetzee MMT. A supplement to the anophelinae of Africa south of the Sahara (Afrotropical Region). Johannesburg: South African Institute for Medical Research; 1987.
20.
go back to reference WHO. Malaria entomology and vector control. Guide for participants. Geneva: World Health Organization; 2013. WHO. Malaria entomology and vector control. Guide for participants. Geneva: World Health Organization; 2013.
21.
go back to reference Bass C, Williamson MS, Field LM. Development of a multiplex real-time PCR assay for identification of members of the Anopheles gambiae species complex. Acta Trop. 2008;107:50–3.CrossRefPubMed Bass C, Williamson MS, Field LM. Development of a multiplex real-time PCR assay for identification of members of the Anopheles gambiae species complex. Acta Trop. 2008;107:50–3.CrossRefPubMed
22.
go back to reference Statacorp. Stata statistical software release 12. College Station: Statacorp LP; 2011. Statacorp. Stata statistical software release 12. College Station: Statacorp LP; 2011.
23.
go back to reference Post RJ, Millest AL. Sample size in parasitological and vector surveys. Parasitol Today. 1991;7:141.CrossRefPubMed Post RJ, Millest AL. Sample size in parasitological and vector surveys. Parasitol Today. 1991;7:141.CrossRefPubMed
24.
go back to reference Manson P, Cook GC, Zumla AI. Manson’s tropical diseases. 22nd ed. Edinburgh: Saunders Elsevier; 2009. Manson P, Cook GC, Zumla AI. Manson’s tropical diseases. 22nd ed. Edinburgh: Saunders Elsevier; 2009.
25.
go back to reference Pennetier C, Bouraima A, Chandre F, Piameu M, Etang J, Rossignol M, et al. Efficacy of Olyset® Plus, a new long-lasting insecticidal net incorporating permethrin and piperonyl-butoxide against multi-resistant malaria vectors [corrected]. PLoS ONE. 2013;8:e75134.CrossRefPubMedPubMedCentral Pennetier C, Bouraima A, Chandre F, Piameu M, Etang J, Rossignol M, et al. Efficacy of Olyset® Plus, a new long-lasting insecticidal net incorporating permethrin and piperonyl-butoxide against multi-resistant malaria vectors [corrected]. PLoS ONE. 2013;8:e75134.CrossRefPubMedPubMedCentral
26.
go back to reference WHO. Guidelines for laboratory and field-testing of long-lasting insecticidal nets. Geneva: World Health Organization; 2013. WHO. Guidelines for laboratory and field-testing of long-lasting insecticidal nets. Geneva: World Health Organization; 2013.
27.
go back to reference Matowo J, Kitau J, Kaaya R, Kavishe R, Wright A, Kisinza W, et al. Trends in the selection of insecticide resistance in Anopheles gambiae s.l. mosquitoes in northwest Tanzania during a community randomized trial of longlasting insecticidal nets and indoor residual spraying. Med Vet Entomol. 2015;29:51–9.CrossRefPubMed Matowo J, Kitau J, Kaaya R, Kavishe R, Wright A, Kisinza W, et al. Trends in the selection of insecticide resistance in Anopheles gambiae s.l. mosquitoes in northwest Tanzania during a community randomized trial of longlasting insecticidal nets and indoor residual spraying. Med Vet Entomol. 2015;29:51–9.CrossRefPubMed
28.
go back to reference Maia MF, Onyango SP, Thele M, Simfukwe ET, Turner EL, Moore SJ. Do topical repellents divert mosquitoes within a community? Health equity implications of topical repellents as a mosquito bite prevention tool. PLoS ONE. 2013;8:e84875.CrossRefPubMedPubMedCentral Maia MF, Onyango SP, Thele M, Simfukwe ET, Turner EL, Moore SJ. Do topical repellents divert mosquitoes within a community? Health equity implications of topical repellents as a mosquito bite prevention tool. PLoS ONE. 2013;8:e84875.CrossRefPubMedPubMedCentral
Metadata
Title
‘Repel all biters’: an enhanced collection of endophilic Anopheles gambiae and Anopheles arabiensis in CDC light-traps, from the Kagera Region of Tanzania, in the presence of a combination mosquito net impregnated with piperonyl butoxide and permethrin
Authors
Corey LeClair
Judith Cronery
Enock Kessy
Elsa V. E. Tomás
Yohannes Kulwa
Franklin W. Mosha
Mark Rowland
Natacha Protopopoff
J. Derek Charlwood
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1972-z

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