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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Evaluation of piperonyl butoxide in enhancing the efficacy of pyrethroid insecticides against resistant Anopheles gambiae s.l. in Ghana

Authors: Samuel K. Dadzie, Joseph Chabi, Andy Asafu-Adjaye, Otubea Owusu-Akrofi, Aba Baffoe-Wilmot, Keziah Malm, Constance Bart-Plange, Sylvester Coleman, Maxwell A. Appawu, Daniel A. Boakye

Published in: Malaria Journal | Issue 1/2017

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Abstract

Background

Malaria vector control methods involving the use of pyrethroids remain the strategies being used against malaria vectors in Ghana. These methods include the use of long-lasting insecticidal nets and indoor residual spraying in many areas in Ghana. However, there is evidence that pyrethroid resistance is widespread in many areas in Ghana. Synergists have been shown to be useful in inhibiting the enzymes that are responsible for the development of resistance and hence enhance the insecticide susceptibility of Anopheles gambiae sensu lato (s.l.) in many areas. The present study investigated the effect of piperonyl butoxide (PBO) on the susceptibility status of An. gambiae s.l. across some sentinel sites in Ghana.

Methods

Three to five day old An. gambiae s.l. reared from larvae were used in WHO susceptibility tube assays. Batches of 20–25 female adult An. gambiae s.l. were exposed simultaneously to the insecticide alone and to the PBO + insecticide. The knock down rate after 60 min and mortality at 24 h were recorded.

Results

Deltamethrin and permethrin resistance of An. gambiae s.l. was observed in all the sites in 2015 and 2016. The mortality after 24 h post exposure for deltamethrin ranged from 16.3% in Weija to 82.3% in Kade, whereas that for permethrin ranged from 3.8% in Gomoa Obuasi to 91.3% in Prestea. A significant increase in susceptibility to deltamethrin and less to permethrin was observed during both 2015 and 2016 years in most of the sites when An. gambiae s.l. mosquitoes were pre-exposed to PBO.

Conclusion

Findings from this study showed that the use of PBO significantly enhanced the susceptibility of An. gambiae s.l. mosquitoes in most of the sentinel sites. It is recommended that vector control strategies incorporating PBO as a synergist can be effective in killing mosquitoes in the presence of deltamethrin and permethrin resistance.
Literature
1.
go back to reference Dabire RK, Diabate A, Baldet T, Pare-Toe L, Guiguemde RT, Ouedraogo JB, et al. Personal protection of long-lasting insecticide-treated nets in areas of Anopheles gambiae s.s. resistance to pyrethroids. Malar J. 2006;5:12.CrossRefPubMedPubMedCentral Dabire RK, Diabate A, Baldet T, Pare-Toe L, Guiguemde RT, Ouedraogo JB, et al. Personal protection of long-lasting insecticide-treated nets in areas of Anopheles gambiae s.s. resistance to pyrethroids. Malar J. 2006;5:12.CrossRefPubMedPubMedCentral
2.
go back to reference N’Guessan R, Corbel V, Akogbeto M, Rowland M. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis. 2007;13:199–206.CrossRefPubMedPubMedCentral N’Guessan R, Corbel V, Akogbeto M, Rowland M. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis. 2007;13:199–206.CrossRefPubMedPubMedCentral
3.
go back to reference Toe KH, Jones CM, N’Fale S, Ismail HM, Dabire RK, Ranson H. Increased pyrethroid resistance in malaria vectors and decreased bed net effectiveness, Burkina Faso. Emerg Infect Dis. 2014;20:1691–6.CrossRefPubMedPubMedCentral Toe KH, Jones CM, N’Fale S, Ismail HM, Dabire RK, Ranson H. Increased pyrethroid resistance in malaria vectors and decreased bed net effectiveness, Burkina Faso. Emerg Infect Dis. 2014;20:1691–6.CrossRefPubMedPubMedCentral
4.
go back to reference Adasi K, Hemingway J. Susceptibility to three pyrethroids and detection of knockdown resistance mutation in Ghanaian Anopheles gambiae sensu stricto. J Vector Ecol. 2008;33:255–62.CrossRefPubMed Adasi K, Hemingway J. Susceptibility to three pyrethroids and detection of knockdown resistance mutation in Ghanaian Anopheles gambiae sensu stricto. J Vector Ecol. 2008;33:255–62.CrossRefPubMed
5.
go back to reference Chabi J, Baidoo PK, Datsomor AK, Okyere D, Ablorde A, Iddrisu A, et al. Insecticide susceptibility of natural populations of Anopheles coluzzii and Anopheles gambiae (sensu stricto) from Okyereko irrigation site, Ghana, West Africa. Parasit Vectors. 2016;9:182.CrossRefPubMedPubMedCentral Chabi J, Baidoo PK, Datsomor AK, Okyere D, Ablorde A, Iddrisu A, et al. Insecticide susceptibility of natural populations of Anopheles coluzzii and Anopheles gambiae (sensu stricto) from Okyereko irrigation site, Ghana, West Africa. Parasit Vectors. 2016;9:182.CrossRefPubMedPubMedCentral
6.
go back to reference Coetzee M, van Wyk P, Booman M, Koekemoer LL, Hunt RH. Insecticide resistance in malaria vector mosquitoes in a gold mining town in Ghana and implications for malaria control. Bull Soc Pathol Exot. 2006;99:400–3.PubMed Coetzee M, van Wyk P, Booman M, Koekemoer LL, Hunt RH. Insecticide resistance in malaria vector mosquitoes in a gold mining town in Ghana and implications for malaria control. Bull Soc Pathol Exot. 2006;99:400–3.PubMed
7.
go back to reference Dery DB, Segbaya S, Asoalla V, Amoyaw F, Amoako N, Agyeman-Budu A, et al. Anopheles gambiae (Diptera: Culicidae) susceptibility to insecticides and knockdown resistance genes prior to introduction of indoor residual spraying in 11 districts in Ghana. J Med Entomol. 2016;53:1403–9.CrossRefPubMed Dery DB, Segbaya S, Asoalla V, Amoyaw F, Amoako N, Agyeman-Budu A, et al. Anopheles gambiae (Diptera: Culicidae) susceptibility to insecticides and knockdown resistance genes prior to introduction of indoor residual spraying in 11 districts in Ghana. J Med Entomol. 2016;53:1403–9.CrossRefPubMed
8.
go back to reference Hunt RH, Fuseini G, Knowles S, Stiles-Ocran J, Verster R, Kaiser ML, et al. Insecticide resistance in malaria vector mosquitoes at four localities in Ghana, West Africa. Parasit Vectors. 2011;4:107.CrossRefPubMedPubMedCentral Hunt RH, Fuseini G, Knowles S, Stiles-Ocran J, Verster R, Kaiser ML, et al. Insecticide resistance in malaria vector mosquitoes at four localities in Ghana, West Africa. Parasit Vectors. 2011;4:107.CrossRefPubMedPubMedCentral
9.
go back to reference Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M. Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg. 2008;102:591–8.CrossRefPubMed Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M. Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg. 2008;102:591–8.CrossRefPubMed
10.
go back to reference Yawson AE, McCall PJ, Wilson MD, Donnelly MJ. Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso. Med Vet Entomol. 2004;18:372–7.CrossRefPubMed Yawson AE, McCall PJ, Wilson MD, Donnelly MJ. Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso. Med Vet Entomol. 2004;18:372–7.CrossRefPubMed
11.
go back to reference Corbel V, Chabi J, Dabire RK, Etang J, Nwane P, Pigeon O, et al. 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. 2010;9:113.CrossRefPubMedPubMedCentral Corbel V, Chabi J, Dabire RK, Etang J, Nwane P, Pigeon O, et al. 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. 2010;9:113.CrossRefPubMedPubMedCentral
12.
go back to reference Pennetier C, Bouraima A, Chandre F, Piameu M, Etang J, Rossignol M, et al. Efficacy of Olyset(R) Plus, a new long-lasting insecticidal net incorporating permethrin and piperonyl-butoxide against multi-resistant malaria vectors. PLoS ONE. 2013;8:e75134.CrossRefPubMedPubMedCentral Pennetier C, Bouraima A, Chandre F, Piameu M, Etang J, Rossignol M, et al. Efficacy of Olyset(R) Plus, a new long-lasting insecticidal net incorporating permethrin and piperonyl-butoxide against multi-resistant malaria vectors. PLoS ONE. 2013;8:e75134.CrossRefPubMedPubMedCentral
13.
go back to reference Bingham G, Gunning RV, Gorman K, Field LM, Moores GD. Temporal synergism by microencapsulation of piperonyl butoxide and alpha-cypermethrin overcomes insecticide resistance in crop pests. Pest Manag Sci. 2007;63:276–81.CrossRefPubMed Bingham G, Gunning RV, Gorman K, Field LM, Moores GD. Temporal synergism by microencapsulation of piperonyl butoxide and alpha-cypermethrin overcomes insecticide resistance in crop pests. Pest Manag Sci. 2007;63:276–81.CrossRefPubMed
14.
go back to reference Moores GD, Philippou D, Borzatta V, Trincia P, Jewess P, Gunning R, Bingham G. An analogue of piperonyl butoxide facilitates the characterisation of metabolic resistance. Pest Manag Sci. 2009;65:150–4.CrossRefPubMed Moores GD, Philippou D, Borzatta V, Trincia P, Jewess P, Gunning R, Bingham G. An analogue of piperonyl butoxide facilitates the characterisation of metabolic resistance. Pest Manag Sci. 2009;65:150–4.CrossRefPubMed
15.
go back to reference Bingham G, Strode C, Tran L, Khoa PT, Jamet HP. Can piperonyl butoxide enhance the efficacy of pyrethroids against pyrethroid-resistant Aedes aegypti? Trop Med Int Health. 2011;16:492–500.CrossRefPubMed Bingham G, Strode C, Tran L, Khoa PT, Jamet HP. Can piperonyl butoxide enhance the efficacy of pyrethroids against pyrethroid-resistant Aedes aegypti? Trop Med Int Health. 2011;16:492–500.CrossRefPubMed
16.
go back to reference Young SJ, Gunning RV, Moores GD. The effect of piperonyl butoxide on pyrethroid-resistance-associated esterases in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Pest Manag Sci. 2005;61:397–401.CrossRefPubMed Young SJ, Gunning RV, Moores GD. The effect of piperonyl butoxide on pyrethroid-resistance-associated esterases in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Pest Manag Sci. 2005;61:397–401.CrossRefPubMed
17.
go back to reference Young SJ, Gunning RV, Moores GD. Effect of pretreatment with piperonyl butoxide on pyrethroid efficacy against insecticide-resistant Helicoverpa armigera (Lepidoptera: Noctuidae) and Bemisia tabaci (Sternorrhyncha: Aleyrodidae). Pest Manag Sci. 2006;62:114–9.CrossRefPubMed Young SJ, Gunning RV, Moores GD. Effect of pretreatment with piperonyl butoxide on pyrethroid efficacy against insecticide-resistant Helicoverpa armigera (Lepidoptera: Noctuidae) and Bemisia tabaci (Sternorrhyncha: Aleyrodidae). Pest Manag Sci. 2006;62:114–9.CrossRefPubMed
18.
go back to reference WHO. Test procedures for insecticide resistance monitoring in malaria vectors mosquitoess. Geneva: World Health Organization; 2013. WHO. Test procedures for insecticide resistance monitoring in malaria vectors mosquitoess. Geneva: World Health Organization; 2013.
19.
go back to reference WHO. Guidelines for laboratory and field testing of long-lasting insecticidal nets. WHO Pesticide Evaluation Scheme (WHOPES); 2013, WHO/HTM/NTD/WHOPES/2013.1. WHO. Guidelines for laboratory and field testing of long-lasting insecticidal nets. WHO Pesticide Evaluation Scheme (WHOPES); 2013, WHO/HTM/NTD/WHOPES/2013.1.
20.
go back to reference Anto F, Asoala V, Anyorigiya T, Oduro A, Adjuik M, Owusu-Agyei S, et al. Insecticide resistance profiles for malaria vectors in the Kassena-Nankana district of Ghana. Malar J. 2009;8:81.CrossRefPubMedPubMedCentral Anto F, Asoala V, Anyorigiya T, Oduro A, Adjuik M, Owusu-Agyei S, et al. Insecticide resistance profiles for malaria vectors in the Kassena-Nankana district of Ghana. Malar J. 2009;8:81.CrossRefPubMedPubMedCentral
21.
go back to reference Chouaibou M, Etang J, Brevault T, Nwane P, Hinzoumbe CK, Mimpfoundi R, et al. Dynamics of insecticide resistance in the malaria vector Anopheles gambiae s.l. from an area of extensive cotton cultivation in Northern Cameroon. Trop Med Int Health. 2008;13:476–86.CrossRefPubMed Chouaibou M, Etang J, Brevault T, Nwane P, Hinzoumbe CK, Mimpfoundi R, et al. Dynamics of insecticide resistance in the malaria vector Anopheles gambiae s.l. from an area of extensive cotton cultivation in Northern Cameroon. Trop Med Int Health. 2008;13:476–86.CrossRefPubMed
22.
go back to reference Cisse MB, Keita C, Dicko A, Dengela D, Coleman J, Lucas B, et al. Characterizing the insecticide resistance of Anopheles gambiae in Mali. Malar J. 2015;14:327.CrossRefPubMedPubMedCentral Cisse MB, Keita C, Dicko A, Dengela D, Coleman J, Lucas B, et al. Characterizing the insecticide resistance of Anopheles gambiae in Mali. Malar J. 2015;14:327.CrossRefPubMedPubMedCentral
23.
go back to reference Corbel V, Hougard JM, N’Guessan R, Chandre F. Evidence for selection of insecticide resistance due to insensitive acetylcholinesterase by carbamate-treated nets in Anopheles gambiae s.s. (Diptera: Culicidae) from Cote d’Ivoire. J Med Entomol. 2003;40:985–8.CrossRefPubMed Corbel V, Hougard JM, N’Guessan R, Chandre F. Evidence for selection of insecticide resistance due to insensitive acetylcholinesterase by carbamate-treated nets in Anopheles gambiae s.s. (Diptera: Culicidae) from Cote d’Ivoire. J Med Entomol. 2003;40:985–8.CrossRefPubMed
24.
go back to reference Corbel V, N’Guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, et al. Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop. 2007;101:207–16.CrossRefPubMed Corbel V, N’Guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, et al. Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop. 2007;101:207–16.CrossRefPubMed
25.
go back to reference Dabire KR, Diabate A, Djogbenou L, Ouari A, N’Guessan R, Ouedraogo JB, et al. Dynamics of multiple insecticide resistance in the malaria vector Anopheles gambiae in a rice growing area in South-Western Burkina Faso. Malar J. 2008;7:188.CrossRefPubMedPubMedCentral Dabire KR, Diabate A, Djogbenou L, Ouari A, N’Guessan R, Ouedraogo JB, et al. Dynamics of multiple insecticide resistance in the malaria vector Anopheles gambiae in a rice growing area in South-Western Burkina Faso. Malar J. 2008;7:188.CrossRefPubMedPubMedCentral
26.
go back to reference Djenontin A, Chabi J, Baldet T, Irish S, Pennetier C, Hougard JM, et al. Managing insecticide resistance in malaria vectors by combining carbamate-treated plastic wall sheeting and pyrethroid-treated bed nets. Malar J. 2009;8:233.CrossRefPubMedPubMedCentral Djenontin A, Chabi J, Baldet T, Irish S, Pennetier C, Hougard JM, et al. Managing insecticide resistance in malaria vectors by combining carbamate-treated plastic wall sheeting and pyrethroid-treated bed nets. Malar J. 2009;8:233.CrossRefPubMedPubMedCentral
27.
go back to reference Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H. Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d’Ivoire. Emerg Infect Dis. 2012;18:1508–11.CrossRefPubMedPubMedCentral Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H. Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d’Ivoire. Emerg Infect Dis. 2012;18:1508–11.CrossRefPubMedPubMedCentral
28.
go back to reference Hemingway J, Ranson H. Insecticide resistance in insect vectors of human disease. Annu Rev Entomol. 2000;45:371–91.CrossRefPubMed Hemingway J, Ranson H. Insecticide resistance in insect vectors of human disease. Annu Rev Entomol. 2000;45:371–91.CrossRefPubMed
29.
go back to reference Ngufor C, N’Guessan R, Fagbohoun J, Subramaniam K, Odjo A, Fongnikin A, et al. Insecticide resistance profile of Anopheles gambiae from a phase II field station in Cove, southern Benin: implications for the evaluation of novel vector control products. Malar J. 2015;14:464.CrossRefPubMedPubMedCentral Ngufor C, N’Guessan R, Fagbohoun J, Subramaniam K, Odjo A, Fongnikin A, et al. Insecticide resistance profile of Anopheles gambiae from a phase II field station in Cove, southern Benin: implications for the evaluation of novel vector control products. Malar J. 2015;14:464.CrossRefPubMedPubMedCentral
30.
go back to reference Perera MD, Hemingway J, Karunaratne SP. Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka. Malar J. 2008;7:168.CrossRefPubMedPubMedCentral Perera MD, Hemingway J, Karunaratne SP. Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka. Malar J. 2008;7:168.CrossRefPubMedPubMedCentral
31.
go back to reference Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbe C, Yangalbe-Kalnone E, et al. Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J. 2009;8:299.CrossRefPubMedPubMedCentral Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbe C, Yangalbe-Kalnone E, et al. Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J. 2009;8:299.CrossRefPubMedPubMedCentral
32.
go back to reference Yadouleton AW, Padonou G, Asidi A, Moiroux N, Bio-Banganna S, Corbel V, et al. Insecticide resistance status in Anopheles gambiae in southern Benin. Malar J. 2010;9:83.CrossRefPubMedPubMedCentral Yadouleton AW, Padonou G, Asidi A, Moiroux N, Bio-Banganna S, Corbel V, et al. Insecticide resistance status in Anopheles gambiae in southern Benin. Malar J. 2010;9:83.CrossRefPubMedPubMedCentral
33.
go back to reference Corbel V, Akogbeto M, Damien GB, Djenontin A, Chandre F, Rogier C, et al. Combination of malaria vector control interventions in pyrethroid resistance area in Benin: a cluster randomised controlled trial. Lancet Infect Dis. 2012;12:617–26.CrossRefPubMed Corbel V, Akogbeto M, Damien GB, Djenontin A, Chandre F, Rogier C, et al. Combination of malaria vector control interventions in pyrethroid resistance area in Benin: a cluster randomised controlled trial. Lancet Infect Dis. 2012;12:617–26.CrossRefPubMed
34.
go back to reference Curtis CF, Jana-Kara B, Maxwell CA. Insecticide treated nets: impact on vector populations and relevance of initial intensity of transmission and pyrethroid resistance. J Vector Borne Dis. 2003;40:1–8.PubMed Curtis CF, Jana-Kara B, Maxwell CA. Insecticide treated nets: impact on vector populations and relevance of initial intensity of transmission and pyrethroid resistance. J Vector Borne Dis. 2003;40:1–8.PubMed
35.
go back to reference Okumu FO, Moore SJ. Combining indoor residual spraying and insecticide-treated nets for malaria control in Africa: a review of possible outcomes and an outline of suggestions for the future. Malar J. 2011;10:208.CrossRefPubMedPubMedCentral Okumu FO, Moore SJ. Combining indoor residual spraying and insecticide-treated nets for malaria control in Africa: a review of possible outcomes and an outline of suggestions for the future. Malar J. 2011;10:208.CrossRefPubMedPubMedCentral
36.
go back to reference Stevens ER, Aldridge A, Degbey Y, Pignandi A, Dorkenoo MA, Hugelen-Padin J. Evaluation of the 2011 long-lasting, insecticide-treated net distribution for universal coverage in Togo. Malar J. 2013;12:162.CrossRefPubMedPubMedCentral Stevens ER, Aldridge A, Degbey Y, Pignandi A, Dorkenoo MA, Hugelen-Padin J. Evaluation of the 2011 long-lasting, insecticide-treated net distribution for universal coverage in Togo. Malar J. 2013;12:162.CrossRefPubMedPubMedCentral
37.
go back to reference Tungu P, Magesa S, Maxwell C, Malima R, Masue D, Sudi W, et al. 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. 2010;9:21.CrossRefPubMedPubMedCentral Tungu P, Magesa S, Maxwell C, Malima R, Masue D, Sudi W, et al. 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. 2010;9:21.CrossRefPubMedPubMedCentral
38.
go back to reference Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH. 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. 2000;9:491–7.CrossRefPubMed Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH. 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. 2000;9:491–7.CrossRefPubMed
39.
go back to reference Ranson H, Jensen B, Wang X, Prapanthadara L, Hemingway J, Collins FH. Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect Mol Biol. 2000;9:499–507.CrossRefPubMed Ranson H, Jensen B, Wang X, Prapanthadara L, Hemingway J, Collins FH. Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect Mol Biol. 2000;9:499–507.CrossRefPubMed
40.
go back to reference Hemingway J, Ranson H, Magill A, Kolaczinski J, Fornadel C, Gimnig J, et al. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet. 2016;387:1785–8.CrossRefPubMed Hemingway J, Ranson H, Magill A, Kolaczinski J, Fornadel C, Gimnig J, et al. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet. 2016;387:1785–8.CrossRefPubMed
41.
go back to reference Lengeler C, Snow RW. From efficacy to effectiveness: insecticide-treated bednets in Africa. Bull World Health Organ. 1996;74:325–32.PubMedPubMedCentral Lengeler C, Snow RW. From efficacy to effectiveness: insecticide-treated bednets in Africa. Bull World Health Organ. 1996;74:325–32.PubMedPubMedCentral
42.
go back to reference Briet OJ, Penny MA, Hardy D, Awolola TS, Van Bortel W, Corbel V, et al. Effects of pyrethroid resistance on the cost effectiveness of a mass distribution of long-lasting insecticidal nets: a modelling study. Malar J. 2013;12:77.CrossRefPubMedPubMedCentral Briet OJ, Penny MA, Hardy D, Awolola TS, Van Bortel W, Corbel V, et al. Effects of pyrethroid resistance on the cost effectiveness of a mass distribution of long-lasting insecticidal nets: a modelling study. Malar J. 2013;12:77.CrossRefPubMedPubMedCentral
43.
go back to reference Kleinschmidt I, Mnzava AP, Kafy HT, Mbogo C, Bashir AI, Bigoga J, et al. Design of a study to determine the impact of insecticide resistance on malaria vector control: a multi-country investigation. Malar J. 2015;14:282.CrossRefPubMedPubMedCentral Kleinschmidt I, Mnzava AP, Kafy HT, Mbogo C, Bashir AI, Bigoga J, et al. Design of a study to determine the impact of insecticide resistance on malaria vector control: a multi-country investigation. Malar J. 2015;14:282.CrossRefPubMedPubMedCentral
44.
go back to reference Darriet F, Chandre F. Combining piperonyl butoxide and dinotefuran restores the efficacy of deltamethrin mosquito nets against resistant Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 2011;48:952–5.CrossRefPubMed Darriet F, Chandre F. Combining piperonyl butoxide and dinotefuran restores the efficacy of deltamethrin mosquito nets against resistant Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 2011;48:952–5.CrossRefPubMed
45.
go back to reference Fakoorziba MR, Eghbal F, Vijayan VA. Synergist efficacy of piperonyl butoxide with deltamethrin as pyrethroid insecticide on Culex tritaeniorhynchus (Diptera: Culicidae) and other mosquitoe species. Environ Toxicol. 2009;24:19–24.CrossRefPubMed Fakoorziba MR, Eghbal F, Vijayan VA. Synergist efficacy of piperonyl butoxide with deltamethrin as pyrethroid insecticide on Culex tritaeniorhynchus (Diptera: Culicidae) and other mosquitoe species. Environ Toxicol. 2009;24:19–24.CrossRefPubMed
46.
go back to reference Kumar S, Thomas A, Sahgal A, Verma A, Samuel T, Pillai MK. Effect of the synergist, piperonyl butoxide, on the development of deltamethrin resistance in yellow fever mosquito, Aedes aegypti L. (Diptera: Culicidae). Arch Insect Biochem Physiol. 2002;50:1–8.CrossRefPubMed Kumar S, Thomas A, Sahgal A, Verma A, Samuel T, Pillai MK. Effect of the synergist, piperonyl butoxide, on the development of deltamethrin resistance in yellow fever mosquito, Aedes aegypti L. (Diptera: Culicidae). Arch Insect Biochem Physiol. 2002;50:1–8.CrossRefPubMed
47.
go back to reference Churcher TS, Lissenden N, Griffin JT, Worrall E, Ranson H. The impact of pyrethroid resistance on the efficacy and effectiveness of bednets for malaria control in Africa. Elife. 2016;5:e16090.CrossRefPubMedPubMedCentral Churcher TS, Lissenden N, Griffin JT, Worrall E, Ranson H. The impact of pyrethroid resistance on the efficacy and effectiveness of bednets for malaria control in Africa. Elife. 2016;5:e16090.CrossRefPubMedPubMedCentral
Metadata
Title
Evaluation of piperonyl butoxide in enhancing the efficacy of pyrethroid insecticides against resistant Anopheles gambiae s.l. in Ghana
Authors
Samuel K. Dadzie
Joseph Chabi
Andy Asafu-Adjaye
Otubea Owusu-Akrofi
Aba Baffoe-Wilmot
Keziah Malm
Constance Bart-Plange
Sylvester Coleman
Maxwell A. Appawu
Daniel A. Boakye
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/s12936-017-1960-3

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The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.