Eisele TP, Larsen DA, Walker N, Cibulskis RE, Yukich JO, Zikusooka CM, Steketee RW, 2012. Estimates of child deaths prevented from malaria prevention scale-up in Africa 2001–2010. Malar J 11: 93.
Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD, 2012. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413–431.
Bhatt S et al., 2015. Coverage and system efficiencies of insecticide-treated nets in Africa from 2000 to 2017. eLife 4: e09672.
Bhatt S et al., 2015. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526: 207–211.
World Health Organization , 2018. World Malaria Report. Geneva, Switzerland: WHO.
Rund SSC, O’Donnell AJ, Gentile JE, Reece SE, 2016. Daily rhythms in mosquitoes and their consequences for malaria transmission. Insects 7: 1–20.
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: 294.
Lengeler C, 2004. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane database of systematic reviews (Online): CD000363.
Larsen DA, Hutchinson P, Bennett A, Yukich J, Anglewicz P, Keating J, Eisele TP, 2014. Community coverage with insecticide-treated mosquito nets and observed associations with all-cause child mortality and malaria parasite infections. Am J Trop Med Hyg 91: 950–958.
Hawley WA et al., 2003. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg 68: 121–127.
Ranson H, Lissenden N, 2016. Insecticide resistance in African Anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends in Parasitology 32: 187--196.
Cisse MBM, Sangare D, Oxborough RM, Dicko A, Dengela D, Sadou A, Mihigo J, George K, Norris L, Fornadel C, 2017. A village level cluster-randomized entomological evaluation of combination long-lasting insecticidal nets containing pyrethroid plus PBO synergist in southern Mali. Malar J 16: 477.
Gleave K, Lissenden N, Richardson M, Choi L, Ranson H, 2018. Piperonyl butoxide (PBO) combined with pyrethroids in insecticide-treated nets to prevent malaria in Africa. Cochrane Database Syst Rev 2018.
Tiono AB et al., 2018. Efficacy of Olyset Duo, a bednet containing pyriproxyfen and permethrin, versus a permethrin-only net against clinical malaria in an area with highly pyrethroid-resistant vectors in rural Burkina Faso: a cluster-randomised controlled trial. Lancet392: 569–580.
Hemingway J, Ranson H, 2000. Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45: 371–391.
Santolamazza F et al., 2008. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 7: 1–8.
Ranson H, N’guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V, 2011. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 91–98.
Hemingway J et al., 2016. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet 387: 1785–1788.
Kelly-Hope L, Ranson H, Hemingway J, 2008. Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis 8: 387–389.
Thomas MB, Read AF, 2016. The threat (or not) of insecticide resistance for malaria control. Proc Natl Acad Sci USA 113: 8900–8902.
Opondo KO, Weetman D, Jawara M, Diatta M, Fofana A, Crombe F, Mwesigwa J, D’Alessandro U, Donnelly MJ, 2016. Does insecticide resistance contribute to heterogeneities in malaria transmission in the Gambia? Malar J 15: 1–10.
Mathanga DP, Mwandama DA, Bauleni A, Chisaka J, Shah MP, Landman KZ, Lindblade KA, Steinhardt LC, 2015. The effectiveness of long-lasting, insecticide-treated nets in a setting of pyrethroid resistance: a case-control study among febrile children 6 to 59 months of age in Machinga District, Malawi. Malar J 14: 1–8.
Kleinschmidt I et al., 2018. Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: a WHO-coordinated, prospective, international, observational cohort study. Lancet Infect Dis 18: 640–649.
Tokponnon FT et al., 2019. Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: evidence from health facility data from Benin. Malar J 18: 1–9.
Bradley J et al., 2017. Insecticide-treated nets provide protection against malaria to children in an area of insecticide resistance in southern Benin. Malar J 16: 1–5.
Ochomo E et al., 2017. Insecticide-treated nets and protection against insecticide- resistant malaria vectors in Western Kenya. Emerg Infect Dis 23: 758–764.
Tusting LS, Bottomley C, Gibson H, Kleinschmidt I, Tatem AJ, Lindsay SW, Gething PW, 2017. Housing improvements and malaria risk in sub-Saharan Africa: a multi-country analysis of survey data. PLoS Med 14: 1–15.
Clarke SE et al., 2001. Do untreated bednets protect against malaria? Trans R Soc Trop Med Hyg 95: 457–462.
Ochomo EO, Bayoh NM, Walker ED, Abongo BO, Ombok MO, Ouma C, Githeko AK, Vulule J, Yan G, Gimnig JE, 2013. The efficacy of long-lasting nets with declining physical integrity may be compromised in areas with high levels of pyrethroid resistance. Malar J 12: 1–10.
Hancock PA, Hendriks CJM, Tangena J-A, Gibson H, Hemingway J, Coleman M, Gething PW, Cameron E, Bhatt S, Moyes CL, 2020. Mapping trends in insecticide resistance phenotypes in African malaria vectors. PLoS Biol 18: e3000633.
Korenromp EL, Armstrong-Schellenberg JRM, Williams BG, Nahlen BL, Snow RW, 2004. Impact of malaria control on childhood anaemia in Africa – a quantitative review. Trop Med Int Health 9: 1050–1065.
Hijmans RJ, van Etten J, 2012. raster: Geographic Analysis and Modeling with Raster Data. Available at: http://cran.univ-lyon1.fr/web/packages/raster/.
R Core Development Team , 2010. R: a language and environment for statistical computing. Available at: http://wwwR-project.org/.
Moyes CL et al., 2019. Analysis-ready datasets for insecticide resistance phenotype and genotype frequency in African malaria vectors. Sci Data 6: 1–11.
Lim SS, Fullman N, Stokes A, Ravishankar N, Masiye F, Murray CJL, Gakidou E, 2011. Net benefits: a multicountry analysis of observational data examining associations between insecticide-treated mosquito nets and health outcomes. PLoS Med 8: e1001091.
Ho DE, Imai K, King G, Stuart EA, 2011. MatchIt: nonparametric preprocessing for parametric causal inference. J Stat Software 42: 1–28.
Ho DE, Imai K, King G, Stuart EA, 2007. Matching as nonparametric preprocessing for reducing model dependence in parametric causal inference. Polit Anal 15: 199–236.
Craig MH, Snow RW, le Sueur D, 1999. A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol Today 15: 105–111.
Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IRF, Johnston GL, Tatem AJ, Hay SI, 2011. A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J 10: 378.
Sinka ME et al., 2011. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis. Parasit Vectors 4: 89.
Viechtbauer W, 2010. Conducting meta-analyses in R with the metafor package. J Stat Software 36: 1–48.
Alout H, Labbé P, Chandre F, Cohuet A, 2017. Malaria vector control still matters despite insecticide resistance. Trends Parasitol 33: 610–618.
Lynd A, Weetman D, Barbosa S, Egyir Yawson A, Mitchell S, Pinto J, Hastings I, Donnelly MJ, 2010. Field, genetic, and modeling approaches show strong positive selection acting upon an insecticide resistance mutation in anopheles gambiae s.s. Mol Biol Evol 27: 1117–1125.
Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, Guillet P, 2000. Modifications of pyrethroid effects associated with kdr mutation in Anophelos gambiae. Med Vet Entomol 14: 81–88.
Viana M, Hughes A, Matthiopoulos J, Ranson H, Ferguson HM, 2016. Delayed mortality effects cut the malaria transmission potential of insecticide-resistant mosquitoes. Proc Natl Acad Sci USA 113: 8975–8980.
Cohnstaedt LW, Allan SA, 2011. Effects of sublethal pyrethroid exposure on the host-seeking behavior of female mosquitoes. J Vector Ecol 36: 395–403.
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Pyrethroid resistance is a major concern for malaria vector control programs that predominantly rely on insecticide-treated mosquito nets (ITNs). Contradictory results of the impact of resistance have been observed during field studies. We combined continent-wide estimates of pyrethroid resistance in Anopheles gambiae from 2006 to 2017, with continent-wide survey data to assess the effect of increasing pyrethroid resistance on the effectiveness of ITNs to prevent malaria infections in sub-Saharan Africa. We used a pooled-data approach and a meta-regression of survey regions to assess how pyrethroid resistance affects the association between ITN ownership and malaria outcomes for children 6 to 59 months of age. ITN ownership reduced the risk of malaria outcomes according to both the pooled and meta-regression approaches. According to the pooled analysis, there was no observed interaction between ITN ownership and estimated level of pyrethroid resistance (likelihood ratio [LR] test, 1.127 for malaria infection confirmed by the rapid diagnostic test, P = 0.2885; LR test = 0.161 for microscopy-confirmed malaria infection, P = 0.161; LR test = 0.646 for moderate or severe anemia, P = 0.4215). Using the meta-regression approach to determine the level of pyrethroid resistance did not explain any of the variance in subnational estimates of ITN effectiveness for any of the outcomes. ITNs decreased the risk of malaria independent of the levels of pyrethroid resistance in malaria vector populations.
Financial support: RLC was supported by a grant from the Syracuse University Office of Undergraduate Research and Creative Engagement (SOURCE).
Authors’ addresses: David A. Larsen and Rachael L. Church, Syracuse University Department of Public Health, Syracuse, NY, E-mails: dalarsen@syr.edu and rchurch@syr.edu.
Eisele TP, Larsen DA, Walker N, Cibulskis RE, Yukich JO, Zikusooka CM, Steketee RW, 2012. Estimates of child deaths prevented from malaria prevention scale-up in Africa 2001–2010. Malar J 11: 93.
Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD, 2012. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413–431.
Bhatt S et al., 2015. Coverage and system efficiencies of insecticide-treated nets in Africa from 2000 to 2017. eLife 4: e09672.
Bhatt S et al., 2015. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526: 207–211.
World Health Organization , 2018. World Malaria Report. Geneva, Switzerland: WHO.
Rund SSC, O’Donnell AJ, Gentile JE, Reece SE, 2016. Daily rhythms in mosquitoes and their consequences for malaria transmission. Insects 7: 1–20.
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: 294.
Lengeler C, 2004. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane database of systematic reviews (Online): CD000363.
Larsen DA, Hutchinson P, Bennett A, Yukich J, Anglewicz P, Keating J, Eisele TP, 2014. Community coverage with insecticide-treated mosquito nets and observed associations with all-cause child mortality and malaria parasite infections. Am J Trop Med Hyg 91: 950–958.
Hawley WA et al., 2003. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg 68: 121–127.
Ranson H, Lissenden N, 2016. Insecticide resistance in African Anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends in Parasitology 32: 187--196.
Cisse MBM, Sangare D, Oxborough RM, Dicko A, Dengela D, Sadou A, Mihigo J, George K, Norris L, Fornadel C, 2017. A village level cluster-randomized entomological evaluation of combination long-lasting insecticidal nets containing pyrethroid plus PBO synergist in southern Mali. Malar J 16: 477.
Gleave K, Lissenden N, Richardson M, Choi L, Ranson H, 2018. Piperonyl butoxide (PBO) combined with pyrethroids in insecticide-treated nets to prevent malaria in Africa. Cochrane Database Syst Rev 2018.
Tiono AB et al., 2018. Efficacy of Olyset Duo, a bednet containing pyriproxyfen and permethrin, versus a permethrin-only net against clinical malaria in an area with highly pyrethroid-resistant vectors in rural Burkina Faso: a cluster-randomised controlled trial. Lancet392: 569–580.
Hemingway J, Ranson H, 2000. Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45: 371–391.
Santolamazza F et al., 2008. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 7: 1–8.
Ranson H, N’guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V, 2011. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 91–98.
Hemingway J et al., 2016. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet 387: 1785–1788.
Kelly-Hope L, Ranson H, Hemingway J, 2008. Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis 8: 387–389.
Thomas MB, Read AF, 2016. The threat (or not) of insecticide resistance for malaria control. Proc Natl Acad Sci USA 113: 8900–8902.
Opondo KO, Weetman D, Jawara M, Diatta M, Fofana A, Crombe F, Mwesigwa J, D’Alessandro U, Donnelly MJ, 2016. Does insecticide resistance contribute to heterogeneities in malaria transmission in the Gambia? Malar J 15: 1–10.
Mathanga DP, Mwandama DA, Bauleni A, Chisaka J, Shah MP, Landman KZ, Lindblade KA, Steinhardt LC, 2015. The effectiveness of long-lasting, insecticide-treated nets in a setting of pyrethroid resistance: a case-control study among febrile children 6 to 59 months of age in Machinga District, Malawi. Malar J 14: 1–8.
Kleinschmidt I et al., 2018. Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: a WHO-coordinated, prospective, international, observational cohort study. Lancet Infect Dis 18: 640–649.
Tokponnon FT et al., 2019. Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: evidence from health facility data from Benin. Malar J 18: 1–9.
Bradley J et al., 2017. Insecticide-treated nets provide protection against malaria to children in an area of insecticide resistance in southern Benin. Malar J 16: 1–5.
Ochomo E et al., 2017. Insecticide-treated nets and protection against insecticide- resistant malaria vectors in Western Kenya. Emerg Infect Dis 23: 758–764.
Tusting LS, Bottomley C, Gibson H, Kleinschmidt I, Tatem AJ, Lindsay SW, Gething PW, 2017. Housing improvements and malaria risk in sub-Saharan Africa: a multi-country analysis of survey data. PLoS Med 14: 1–15.
Clarke SE et al., 2001. Do untreated bednets protect against malaria? Trans R Soc Trop Med Hyg 95: 457–462.
Ochomo EO, Bayoh NM, Walker ED, Abongo BO, Ombok MO, Ouma C, Githeko AK, Vulule J, Yan G, Gimnig JE, 2013. The efficacy of long-lasting nets with declining physical integrity may be compromised in areas with high levels of pyrethroid resistance. Malar J 12: 1–10.
Hancock PA, Hendriks CJM, Tangena J-A, Gibson H, Hemingway J, Coleman M, Gething PW, Cameron E, Bhatt S, Moyes CL, 2020. Mapping trends in insecticide resistance phenotypes in African malaria vectors. PLoS Biol 18: e3000633.
Korenromp EL, Armstrong-Schellenberg JRM, Williams BG, Nahlen BL, Snow RW, 2004. Impact of malaria control on childhood anaemia in Africa – a quantitative review. Trop Med Int Health 9: 1050–1065.
Hijmans RJ, van Etten J, 2012. raster: Geographic Analysis and Modeling with Raster Data. Available at: http://cran.univ-lyon1.fr/web/packages/raster/.
R Core Development Team , 2010. R: a language and environment for statistical computing. Available at: http://wwwR-project.org/.
Moyes CL et al., 2019. Analysis-ready datasets for insecticide resistance phenotype and genotype frequency in African malaria vectors. Sci Data 6: 1–11.
Lim SS, Fullman N, Stokes A, Ravishankar N, Masiye F, Murray CJL, Gakidou E, 2011. Net benefits: a multicountry analysis of observational data examining associations between insecticide-treated mosquito nets and health outcomes. PLoS Med 8: e1001091.
Ho DE, Imai K, King G, Stuart EA, 2011. MatchIt: nonparametric preprocessing for parametric causal inference. J Stat Software 42: 1–28.
Ho DE, Imai K, King G, Stuart EA, 2007. Matching as nonparametric preprocessing for reducing model dependence in parametric causal inference. Polit Anal 15: 199–236.
Craig MH, Snow RW, le Sueur D, 1999. A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol Today 15: 105–111.
Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IRF, Johnston GL, Tatem AJ, Hay SI, 2011. A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J 10: 378.
Sinka ME et al., 2011. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis. Parasit Vectors 4: 89.
Viechtbauer W, 2010. Conducting meta-analyses in R with the metafor package. J Stat Software 36: 1–48.
Alout H, Labbé P, Chandre F, Cohuet A, 2017. Malaria vector control still matters despite insecticide resistance. Trends Parasitol 33: 610–618.
Lynd A, Weetman D, Barbosa S, Egyir Yawson A, Mitchell S, Pinto J, Hastings I, Donnelly MJ, 2010. Field, genetic, and modeling approaches show strong positive selection acting upon an insecticide resistance mutation in anopheles gambiae s.s. Mol Biol Evol 27: 1117–1125.
Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, Guillet P, 2000. Modifications of pyrethroid effects associated with kdr mutation in Anophelos gambiae. Med Vet Entomol 14: 81–88.
Viana M, Hughes A, Matthiopoulos J, Ranson H, Ferguson HM, 2016. Delayed mortality effects cut the malaria transmission potential of insecticide-resistant mosquitoes. Proc Natl Acad Sci USA 113: 8975–8980.
Cohnstaedt LW, Allan SA, 2011. Effects of sublethal pyrethroid exposure on the host-seeking behavior of female mosquitoes. J Vector Ecol 36: 395–403.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 741 | 307 | 5 |
Full Text Views | 340 | 39 | 10 |
PDF Downloads | 283 | 24 | 0 |