Skip to main content
Top
Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

Do holes in long-lasting insecticidal nets compromise their efficacy against pyrethroid resistant Anopheles gambiae and Culex quinquefasciatus? Results from a release–recapture study in experimental huts

Authors: Sanjiarizaha Randriamaherijaona, Olivier J T Briët, Sébastien Boyer, Aziz Bouraima, Raphael N’Guessan, Christophe Rogier, Vincent Corbel

Published in: Malaria Journal | Issue 1/2015

Login to get access

Abstract

Background

Resistance of malaria vectors to pyrethroids threatens the effectiveness of long-lasting insecticidal nets (LLINs) as a tool for malaria control. Recent experimental hut and observational studies in Benin show that pyrethroid resistance reduces the insecticidal effect and personal protection of LLINs especially when they become torn. The World Health Organization has proposed a threshold for when nets are “too torn” at 1,000 cm2 for rectangular holes and 790 cm2 for round holes. This study examines whether there is a threshold above which LLINs no longer reduce malaria transmission.

Methods

Intact and artificially-holed LLINs under three months old and untreated nets were tested by releasing mosquitoes from a susceptible Anopheles gambiae colony, a pyrethroid-resistant An. gambiae population and a resistant Culex quinquefasciatus population in closed experimental huts in Southern Benin, West Africa. The efficacy of LLINs and untreated nets was evaluated in terms of protection against blood feeding, insecticidal effect and potential effect on malaria transmission.

Results

Personal protection by both LLINs and untreated nets decreased exponentially with increasing holed surface area, without evidence for a specific threshold beyond which LLINs could be considered as ineffective. The insecticidal effect of LLINs was lower in resistant mosquitoes than in susceptible mosquitoes, but holed surface area had little or no impact on the insecticidal effect of LLINs. LLINs with 22,500 cm2 holed surface area and target insecticide content provided a personal protection of 0.60 (95 % CI 0.44–0.73) and a low insecticidal effect of 0.20 (95 % CI 0.12–0.30) against resistant An. gambiae. Nevertheless, mathematical models suggested that if 80 % of the population uses such nets, they could still prevent 94 % (95 % CI 89–97 %) of transmission by pyrethroid-resistant An. gambiae.

Conclusions

Even though personal protection by LLINs against feeding mosquitoes is strongly reduced by holes, the insecticidal effect of LLINs is independent of the holed surface area, but strongly dependent on insecticide resistance. Badly torn nets that still contain insecticide have potential to reduce malaria transmission. The relationship between LLIN integrity and efficacy needs to be understood in order to guide LLIN distribution policy.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO (2013) World malaria report. World Health Organization, Geneva WHO (2013) World malaria report. World Health Organization, Geneva
2.
3.
go back to reference Okumu FO, Kiware SS, Moore SJ, Killeen GF (2013) Mathematical evaluation of community level impact of combining bed nets and indoor residual spraying upon malaria transmission in areas where the main vectors are Anopheles arabiensis mosquitoes. Parasit Vectors 6:17PubMedCentralCrossRefPubMed Okumu FO, Kiware SS, Moore SJ, Killeen GF (2013) Mathematical evaluation of community level impact of combining bed nets and indoor residual spraying upon malaria transmission in areas where the main vectors are Anopheles arabiensis mosquitoes. Parasit Vectors 6:17PubMedCentralCrossRefPubMed
4.
go back to reference Corbel V, N’Guessan R (2013) Distribution, mechanisms, impact and management of insecticide resistance in malaria vectors: a pragmatic review. In: Manguin S (ed) Anopheles mosquitoes—new insights into malaria vectors: InTech, pp 579–633 Corbel V, N’Guessan R (2013) Distribution, mechanisms, impact and management of insecticide resistance in malaria vectors: a pragmatic review. In: Manguin S (ed) Anopheles mosquitoes—new insights into malaria vectors: InTech, pp 579–633
5.
go back to reference Chandre F, Darriet F, Darder M, Cuany A, Doannio JMC, Pasteur N et al (1998) Pyrethroid resistance in Culex quinquefasciatus from West Africa. Med Vet Entomol 12:359–366CrossRefPubMed Chandre F, Darriet F, Darder M, Cuany A, Doannio JMC, Pasteur N et al (1998) Pyrethroid resistance in Culex quinquefasciatus from West Africa. Med Vet Entomol 12:359–366CrossRefPubMed
6.
go back to reference Corbel V, N’guessan R, Brengues C, Chandre F, Djogbenou L, Martin T et al (2007) Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop 101:207–216CrossRefPubMed Corbel V, N’guessan R, Brengues C, Chandre F, Djogbenou L, Martin T et al (2007) Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop 101:207–216CrossRefPubMed
8.
go back to reference Moiroux N, Gomez MB, Pennetier C, Elanga E, Djénontin A, Chandre F et al (2012) Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis 206:1622–1629CrossRefPubMed Moiroux N, Gomez MB, Pennetier C, Elanga E, Djénontin A, Chandre F et al (2012) Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis 206:1622–1629CrossRefPubMed
9.
go back to reference Mwangi TW, Ross A, Marsh K, Snow RW (2003) The effects of untreated bednets on malaria infection and morbidity on the Kenyan coast. Trans R Soc Trop Med Hyg 97:369–372CrossRefPubMed Mwangi TW, Ross A, Marsh K, Snow RW (2003) The effects of untreated bednets on malaria infection and morbidity on the Kenyan coast. Trans R Soc Trop Med Hyg 97:369–372CrossRefPubMed
10.
go back to reference Port GR, Boreham PFL (1982) The effect of bed nets on feeding by Anopheles gambiae Giles (Diptera, Culicidae). Bull Entomol Res 72:483–488CrossRef Port GR, Boreham PFL (1982) The effect of bed nets on feeding by Anopheles gambiae Giles (Diptera, Culicidae). Bull Entomol Res 72:483–488CrossRef
12.
go back to reference Darriet F, Robert V, Vien NT, Carnevale P (1984) Evaluation de l’efficacité sur les vecteurs du paludisme de la perméthrine en imprégnation sur des moustiquaires intactes et trouées. Report no.: WHO/VBC/84.899, pp 19 Darriet F, Robert V, Vien NT, Carnevale P (1984) Evaluation de l’efficacité sur les vecteurs du paludisme de la perméthrine en imprégnation sur des moustiquaires intactes et trouées. Report no.: WHO/VBC/84.899, pp 19
13.
go back to reference Carnevale P, Bitsindou P, Diomande L, Robert V (1992) Insecticide impregnation can restore the efficiency of torn bed nets and reduce man-vector contact in malaria endemic areas. Trans R Soc Trop Med Hyg 86:362–364CrossRefPubMed Carnevale P, Bitsindou P, Diomande L, Robert V (1992) Insecticide impregnation can restore the efficiency of torn bed nets and reduce man-vector contact in malaria endemic areas. Trans R Soc Trop Med Hyg 86:362–364CrossRefPubMed
14.
go back to reference Irish SR, N’Guessan R, Boko PM, Metonnou C, Odjo A, Akogbeto M et al (2008) Loss of protection with insecticide-treated nets against pyrethroid-resistant Culex quinquefasciatus mosquitoes once nets become holed: an experimental hut study. Parasit Vectors 1:17PubMedCentralCrossRefPubMed Irish SR, N’Guessan R, Boko PM, Metonnou C, Odjo A, Akogbeto M et al (2008) Loss of protection with insecticide-treated nets against pyrethroid-resistant Culex quinquefasciatus mosquitoes once nets become holed: an experimental hut study. Parasit Vectors 1:17PubMedCentralCrossRefPubMed
15.
go back to reference Asidi A, N’Guessan R, Akogbeto M, Curtis C, Rowland M (2012) Loss of household protection from use of insecticide-treated nets against pyrethroid-resistant mosquitoes, Benin. Emerg Infect Dis 18:1101PubMedCentralCrossRefPubMed Asidi A, N’Guessan R, Akogbeto M, Curtis C, Rowland M (2012) Loss of household protection from use of insecticide-treated nets against pyrethroid-resistant mosquitoes, Benin. Emerg Infect Dis 18:1101PubMedCentralCrossRefPubMed
16.
go back to reference WHO (2013) Guidelines for laboratory and field-testing of long-lasting insecticidal nets. World Health Organization, Geneva WHO (2013) Guidelines for laboratory and field-testing of long-lasting insecticidal nets. World Health Organization, Geneva
17.
go back to reference Mutuku FM, Khambira M, Bisanzio D, Mungai P, Mwanzo I, Muchiri EM et al (2013) Physical condition and maintenance of mosquito bed nets in Kwale County, coastal Kenya. Malar J 12:46PubMedCentralCrossRefPubMed Mutuku FM, Khambira M, Bisanzio D, Mungai P, Mwanzo I, Muchiri EM et al (2013) Physical condition and maintenance of mosquito bed nets in Kwale County, coastal Kenya. Malar J 12:46PubMedCentralCrossRefPubMed
18.
go back to reference VCTEG (2013) Vector Control Technical Expert Group Report to MPAC: Estimating functional survival of long-lasting insecticidal nets from field data. Geneva VCTEG (2013) Vector Control Technical Expert Group Report to MPAC: Estimating functional survival of long-lasting insecticidal nets from field data. Geneva
19.
go back to reference Chitnis N, Smith T, Steketee R (2008) A mathematical model for the dynamics of malaria in mosquitoes feeding on a heterogeneous host population. J Biol Dyn 2:259–285CrossRefPubMed Chitnis N, Smith T, Steketee R (2008) A mathematical model for the dynamics of malaria in mosquitoes feeding on a heterogeneous host population. J Biol Dyn 2:259–285CrossRefPubMed
20.
go back to reference Briët OJT, Penny MA, Hardy D, Awolola TS, Van Bortel W, Corbel V et al (2013) Effects of pyrethroid resistance on the cost effectiveness of a mass distribution of long-lasting insecticidal nets: a modelling study. Malar J 12:77PubMedCentralCrossRefPubMed Briët OJT, Penny MA, Hardy D, Awolola TS, Van Bortel W, Corbel V et al (2013) Effects of pyrethroid resistance on the cost effectiveness of a mass distribution of long-lasting insecticidal nets: a modelling study. Malar J 12:77PubMedCentralCrossRefPubMed
21.
go back to reference Vulule JM, Beach RF, Atieli FK, Roberts JM, Mount DL, Mwangi RW (1994) Reduced susceptibility of Anopheles gambiae to permethrin associated with the use of permethrin impregnated bednets and curtains in Kenya. Med Vet Entomol 8:71–75CrossRefPubMed Vulule JM, Beach RF, Atieli FK, Roberts JM, Mount DL, Mwangi RW (1994) Reduced susceptibility of Anopheles gambiae to permethrin associated with the use of permethrin impregnated bednets and curtains in Kenya. Med Vet Entomol 8:71–75CrossRefPubMed
22.
go back to reference Yadouleton AW, Padonou G, Asidi A, Moiroux N, Bio-Banganna S, Corbel V et al (2010) Insecticide resistance status in Anopheles gambiae in southern Benin. Malar J 9:83PubMedCentralCrossRefPubMed Yadouleton AW, Padonou G, Asidi A, Moiroux N, Bio-Banganna S, Corbel V et al (2010) Insecticide resistance status in Anopheles gambiae in southern Benin. Malar J 9:83PubMedCentralCrossRefPubMed
23.
go back to reference Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, Hemingway J et al (2008) Expression of the cytochrome P450 s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae ss from Southern Benin and Nigeria. BMC Genom 9:538CrossRef Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, Hemingway J et al (2008) Expression of the cytochrome P450 s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae ss from Southern Benin and Nigeria. BMC Genom 9:538CrossRef
24.
go back to reference WHO (1998) Test procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces. WHO, Geneva WHO (1998) Test procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces. WHO, Geneva
25.
go back to reference WHO (2009) Report of the thirteenth WHOPES working group meeting. World Health Organization, Geneva WHO (2009) Report of the thirteenth WHOPES working group meeting. World Health Organization, Geneva
27.
go back to reference Tungu P, Magesa S, Maxwell C, Malima R, Masue D, Sudi W et al (2010) Evaluation of PermaNet 3.0 a deltamethrin-PBO combination net against Anopheles gambiae and pyrethroid resistant Culex quinquefasciatus mosquitoes: an experimental hut trial in Tanzania. Malar J 9:21PubMedCentralCrossRefPubMed Tungu P, Magesa S, Maxwell C, Malima R, Masue D, Sudi W et al (2010) Evaluation of PermaNet 3.0 a deltamethrin-PBO combination net against Anopheles gambiae and pyrethroid resistant Culex quinquefasciatus mosquitoes: an experimental hut trial in Tanzania. Malar J 9:21PubMedCentralCrossRefPubMed
28.
go back to reference Kabula B, Tungu P, Matowo J, Kitau J, Mweya C, Emidi B et al (2010) Susceptibility status of malaria vectors to insecticides commonly used for malaria control in Tanzania. Trop Med Int Health 17:742–750CrossRef Kabula B, Tungu P, Matowo J, Kitau J, Mweya C, Emidi B et al (2010) Susceptibility status of malaria vectors to insecticides commonly used for malaria control in Tanzania. Trop Med Int Health 17:742–750CrossRef
29.
go back to reference N’Guessan R, Asidi A, Boko P, Odjo A, Akogbeto M, Pigeon O et al (2010) An experimental hut evaluation of PermaNet® 3.0, a deltamethrin-piperonyl butoxide combination net, against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes in southern Benin. Trans R Soc Trop Med Hyg 104:758–765CrossRefPubMed N’Guessan R, Asidi A, Boko P, Odjo A, Akogbeto M, Pigeon O et al (2010) An experimental hut evaluation of PermaNet® 3.0, a deltamethrin-piperonyl butoxide combination net, against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes in southern Benin. Trans R Soc Trop Med Hyg 104:758–765CrossRefPubMed
30.
go back to reference Corbel V, Chabi J, Dabire RK, Etang J, Nwane P, Pigeon O et al (2010) Field efficacy of a new mosaic long-lasting mosquito net (PermaNet 3.0) against pyrethroid-resistant malaria vectors: a multi centre study in Western and Central Africa. Malar J 9:113. doi:10.1186/1475-2875-9-113 PubMedCentralCrossRefPubMed Corbel V, Chabi J, Dabire RK, Etang J, Nwane P, Pigeon O et al (2010) Field efficacy of a new mosaic long-lasting mosquito net (PermaNet 3.0) against pyrethroid-resistant malaria vectors: a multi centre study in Western and Central Africa. Malar J 9:113. doi:10.​1186/​1475-2875-9-113 PubMedCentralCrossRefPubMed
31.
go back to reference Mosha FW, Lyimo IN, Oxborough RM, Matowo J, Malima R, Feston E et al (2008) Comparative efficacies of permethrin-, deltamethrin-and alpha-cypermethrin-treated nets, against Anopheles arabiensis and Culex quinquefasciatus in northern Tanzania. Ann Trop Med Parasitol 102:367–376CrossRefPubMed Mosha FW, Lyimo IN, Oxborough RM, Matowo J, Malima R, Feston E et al (2008) Comparative efficacies of permethrin-, deltamethrin-and alpha-cypermethrin-treated nets, against Anopheles arabiensis and Culex quinquefasciatus in northern Tanzania. Ann Trop Med Parasitol 102:367–376CrossRefPubMed
32.
go back to reference Chitnis N, Hyman JM, Cushing JM (2008) Determining important parameters in the spread of malaria through the sensitivity analysis of a mathematical model. Bull Math Biol 70:1272–1296CrossRefPubMed Chitnis N, Hyman JM, Cushing JM (2008) Determining important parameters in the spread of malaria through the sensitivity analysis of a mathematical model. Bull Math Biol 70:1272–1296CrossRefPubMed
33.
go back to reference Plummer M (ed) (2003) JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. Austria, Vienna Plummer M (ed) (2003) JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. Austria, Vienna
35.
go back to reference Irish SR (2014) The behaviour of mosquitoes in relation to humans under holed bednets: the evidence from experimental huts. Mem Inst Oswaldo Cruz 109:905–911PubMedCentralCrossRefPubMed Irish SR (2014) The behaviour of mosquitoes in relation to humans under holed bednets: the evidence from experimental huts. Mem Inst Oswaldo Cruz 109:905–911PubMedCentralCrossRefPubMed
36.
go back to reference Ngufor C, N’Guessan R, Boko P, Odjo A, Vigninou E, Asidi A et al (2011) Combining indoor residual spraying with chlorfenapyr and long-lasting insecticidal bed nets for improved control of pyrethroid-resistant Anopheles gambiae: an experimental hut trial in Benin. Malar J 10:343PubMedCentralCrossRefPubMed Ngufor C, N’Guessan R, Boko P, Odjo A, Vigninou E, Asidi A et al (2011) Combining indoor residual spraying with chlorfenapyr and long-lasting insecticidal bed nets for improved control of pyrethroid-resistant Anopheles gambiae: an experimental hut trial in Benin. Malar J 10:343PubMedCentralCrossRefPubMed
37.
go back to reference Asidi AN, N’Guessan R, Koffi AA, Curtis CF, Hougard JM, Chandre F et al (2005) Experimental hut evaluation of bednets treated with an organophosphate (chlorpyrifos-methyl) or a pyrethroid (lambdacyhalothrin) alone and in combination against insecticide-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes. Malar J 4:25. doi:10.1186/1475-2875-4-25 PubMedCentralCrossRefPubMed Asidi AN, N’Guessan R, Koffi AA, Curtis CF, Hougard JM, Chandre F et al (2005) Experimental hut evaluation of bednets treated with an organophosphate (chlorpyrifos-methyl) or a pyrethroid (lambdacyhalothrin) alone and in combination against insecticide-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes. Malar J 4:25. doi:10.​1186/​1475-2875-4-25 PubMedCentralCrossRefPubMed
38.
go back to reference Curtis CF, Myamba J, Wilkes TJ (1992) Various pyrethroids on bednets and curtains. Mem Inst Oswaldo Cruz 87(Suppl 3):363–370CrossRefPubMed Curtis CF, Myamba J, Wilkes TJ (1992) Various pyrethroids on bednets and curtains. Mem Inst Oswaldo Cruz 87(Suppl 3):363–370CrossRefPubMed
39.
go back to reference Curtis CF, Myamba J, Wilkes TJ (1996) Comparison of different insecticides and fabrics for anti-mosquito bednets and curtains. Med Vet Entomol 10:1–11CrossRefPubMed Curtis CF, Myamba J, Wilkes TJ (1996) Comparison of different insecticides and fabrics for anti-mosquito bednets and curtains. Med Vet Entomol 10:1–11CrossRefPubMed
40.
go back to reference Lines J, Curtis C, Myamba J, Njau R (1985) Tests of repellent or insecticide impregnated curtains, bednets and anklets against malaria vectors in Tanzania. World Health Organization, Geneva Lines J, Curtis C, Myamba J, Njau R (1985) Tests of repellent or insecticide impregnated curtains, bednets and anklets against malaria vectors in Tanzania. World Health Organization, Geneva
41.
go back to reference Morgan J, Abilio AP, do Rosario Pondja M, Marrenjo D, Luciano J, Fernandes G et al (2015) Physical durability of two types of long-lasting insecticidal nets (LLINs) 3 years after a mass LLIN distribution campaign in Mozambique, 2008–2011. Am J Trop Med Hyg. 92:286–293. doi:10.4269/ajtmh.14-0023 CrossRefPubMed Morgan J, Abilio AP, do Rosario Pondja M, Marrenjo D, Luciano J, Fernandes G et al (2015) Physical durability of two types of long-lasting insecticidal nets (LLINs) 3 years after a mass LLIN distribution campaign in Mozambique, 2008–2011. Am J Trop Med Hyg. 92:286–293. doi:10.​4269/​ajtmh.​14-0023 CrossRefPubMed
42.
go back to reference Lynd A, McCall PJ (2013) Clustering of host-seeking activity of Anopheles gambiae mosquitoes at the top surface of a human-baited bed net. Malar J 12:267PubMedCentralCrossRefPubMed Lynd A, McCall PJ (2013) Clustering of host-seeking activity of Anopheles gambiae mosquitoes at the top surface of a human-baited bed net. Malar J 12:267PubMedCentralCrossRefPubMed
43.
go back to reference Sutcliffe JF, Yin S (2014) Behavioural responses of females of two anopheline mosquito species to human-occupied, insecticide-treated and untreated bed nets. Malar J 13:294PubMedCentralCrossRefPubMed Sutcliffe JF, Yin S (2014) Behavioural responses of females of two anopheline mosquito species to human-occupied, insecticide-treated and untreated bed nets. Malar J 13:294PubMedCentralCrossRefPubMed
44.
go back to reference Boreham PFL, Port GR (1982) The distribution and movement of engorged females of Anopheles gambiae Giles (Diptera, Culicidae) in a Gambian village. Bull Entomol Res 72:489–495CrossRef Boreham PFL, Port GR (1982) The distribution and movement of engorged females of Anopheles gambiae Giles (Diptera, Culicidae) in a Gambian village. Bull Entomol Res 72:489–495CrossRef
45.
go back to reference Gokool S, Smith DF, Curtis CF (1992) The use of PCR to help quantify the protection provided by impregnated bednets. Parasitol Today 8:347–350CrossRefPubMed Gokool S, Smith DF, Curtis CF (1992) The use of PCR to help quantify the protection provided by impregnated bednets. Parasitol Today 8:347–350CrossRefPubMed
46.
go back to reference Gokool S, Curtis CF, Smith DF (1993) Analysis of mosquito bloodmeals by DNA profiling. Med Vet Entomol 7:208–215CrossRefPubMed Gokool S, Curtis CF, Smith DF (1993) Analysis of mosquito bloodmeals by DNA profiling. Med Vet Entomol 7:208–215CrossRefPubMed
47.
go back to reference Smith A, Webley DJ (1969) A verandah-trap hut for studying the house-frequenting habits of mosquitoes and for assessing insecticides. 3. The effect of DDT on behavior and mortality. Bull Entomol Res 59:33–46CrossRefPubMed Smith A, Webley DJ (1969) A verandah-trap hut for studying the house-frequenting habits of mosquitoes and for assessing insecticides. 3. The effect of DDT on behavior and mortality. Bull Entomol Res 59:33–46CrossRefPubMed
48.
go back to reference Edman JD, Bidlingm WL (1969) Flight capacity of blood-engorged mosquitoes. Mosq News 29:386–392 Edman JD, Bidlingm WL (1969) Flight capacity of blood-engorged mosquitoes. Mosq News 29:386–392
51.
go back to reference Kilian A, Byamukama W, Pigeon O, Atieli F, Duchon S, Phan C (2008) Long-term field performance of a polyester-based long-lasting insecticidal mosquito net in rural Uganda. Malar J 7:49PubMedCentralCrossRefPubMed Kilian A, Byamukama W, Pigeon O, Atieli F, Duchon S, Phan C (2008) Long-term field performance of a polyester-based long-lasting insecticidal mosquito net in rural Uganda. Malar J 7:49PubMedCentralCrossRefPubMed
52.
go back to reference Kilian A, Byamukama W, Pigeon O, Gimnig J, Atieli F, Koekemoer L et al (2011) Evidence for a useful life of more than 3 years for a polyester-based long-lasting insecticidal mosquito net in Western Uganda. Malar J 10:299PubMedCentralCrossRefPubMed Kilian A, Byamukama W, Pigeon O, Gimnig J, Atieli F, Koekemoer L et al (2011) Evidence for a useful life of more than 3 years for a polyester-based long-lasting insecticidal mosquito net in Western Uganda. Malar J 10:299PubMedCentralCrossRefPubMed
53.
go back to reference Maxwell CA, Msuya E, Sudi M, Njunwa KJ, Carneiro IA, Curtis CF (2002) Effect of community-wide use of insecticide-treated nets for 3–4 years on malarial morbidity in Tanzania. Trop Med Int Health 7:1003–1008CrossRefPubMed Maxwell CA, Msuya E, Sudi M, Njunwa KJ, Carneiro IA, Curtis CF (2002) Effect of community-wide use of insecticide-treated nets for 3–4 years on malarial morbidity in Tanzania. Trop Med Int Health 7:1003–1008CrossRefPubMed
55.
go back to reference WHO (2013) WHO recommendations for achieving universal coverage with long-lasting insecticidal nets in malaria control. World Health Organization, Geneva (revised March 2014) WHO (2013) WHO recommendations for achieving universal coverage with long-lasting insecticidal nets in malaria control. World Health Organization, Geneva (revised March 2014)
56.
go back to reference WHO (2006) Guidelines for testing mosquito adulticides for indoor residual spraying and treatment of mosquito nets. World Health Organization, Geneva WHO (2006) Guidelines for testing mosquito adulticides for indoor residual spraying and treatment of mosquito nets. World Health Organization, Geneva
58.
go back to reference Killeen GF, Smith TA (2007) Exploring the contributions of bed nets, cattle, insecticides and excitorepellency to malaria control: a deterministic model of mosquito host-seeking behaviour and mortality. Trans R Soc Trop Med Hyg 101:867–880PubMedCentralCrossRefPubMed Killeen GF, Smith TA (2007) Exploring the contributions of bed nets, cattle, insecticides and excitorepellency to malaria control: a deterministic model of mosquito host-seeking behaviour and mortality. Trans R Soc Trop Med Hyg 101:867–880PubMedCentralCrossRefPubMed
59.
go back to reference Le Menach A, Takala S, McKenzie FE, Perisse A, Harris A, Flahault A et al (2007) An elaborated feeding cycle model for reductions in vectorial capacity of night-biting mosquitoes by insecticide-treated nets. Malar J 6:10PubMedCentralCrossRefPubMed Le Menach A, Takala S, McKenzie FE, Perisse A, Harris A, Flahault A et al (2007) An elaborated feeding cycle model for reductions in vectorial capacity of night-biting mosquitoes by insecticide-treated nets. Malar J 6:10PubMedCentralCrossRefPubMed
60.
go back to reference Koudou BG, Koffi AA, Malone D, Hemingway J (2011) Efficacy of PermaNet® 2.0 and PermaNet® 3.0 against insecticide-resistant Anopheles gambiae in experimental huts in Côte d’Ivoire. Malar J 10:172PubMedCentralCrossRefPubMed Koudou BG, Koffi AA, Malone D, Hemingway J (2011) Efficacy of PermaNet® 2.0 and PermaNet® 3.0 against insecticide-resistant Anopheles gambiae in experimental huts in Côte d’Ivoire. Malar J 10:172PubMedCentralCrossRefPubMed
Metadata
Title
Do holes in long-lasting insecticidal nets compromise their efficacy against pyrethroid resistant Anopheles gambiae and Culex quinquefasciatus? Results from a release–recapture study in experimental huts
Authors
Sanjiarizaha Randriamaherijaona
Olivier J T Briët
Sébastien Boyer
Aziz Bouraima
Raphael N’Guessan
Christophe Rogier
Vincent Corbel
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0836-7

Other articles of this Issue 1/2015

Malaria Journal 1/2015 Go to the issue