The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis

Pyrethroid insecticide-treated bed nets (ITNs) help contribute to reducing malaria deaths in Africa, but their efficacy is threatened by insecticide resistance in some malaria mosquito vectors. We therefore assessed the evidence that resistance is attenuating the effect of ITNs on entomological outc...

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Veröffentlicht in:PLoS medicine 2014-03, Vol.11 (3), p.e1001619
Hauptverfasser: Strode, Clare, Donegan, Sarah, Garner, Paul, Enayati, Ahmad Ali, Hemingway, Janet
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description Pyrethroid insecticide-treated bed nets (ITNs) help contribute to reducing malaria deaths in Africa, but their efficacy is threatened by insecticide resistance in some malaria mosquito vectors. We therefore assessed the evidence that resistance is attenuating the effect of ITNs on entomological outcomes. We included laboratory and field studies of African malaria vectors that measured resistance at the time of the study and used World Health Organization-recommended impregnation regimens. We reported mosquito mortality, blood feeding, induced exophily (premature exit of mosquitoes from the hut), deterrence, time to 50% or 95% knock-down, and percentage knock-down at 60 min. Publications were searched from 1 January 1980 to 31 December 2013 using MEDLINE, Cochrane Central Register of Controlled Trials, Science Citation Index Expanded, Social Sciences Citation Index, African Index Medicus, and CAB Abstracts. We stratified studies into three levels of insecticide resistance, and ITNs were compared with untreated bed nets (UTNs) using the risk difference (RD). Heterogeneity was explored visually and statistically. Included were 36 laboratory and 24 field studies, reported in 25 records. Studies tested and reported resistance inconsistently. Based on the meta-analytic results, the difference in mosquito mortality risk for ITNs compared to UTNs was lower in higher resistance categories. However, mortality risk was significantly higher for ITNs compared to UTNs regardless of resistance. For cone tests: low resistance, risk difference (RD) 0.86 (95% CI 0.72 to 1.01); moderate resistance, RD 0.71 (95% CI 0.53 to 0.88); high resistance, RD 0.56 (95% CI 0.17 to 0.95). For tunnel tests: low resistance, RD 0.74 (95% CI 0.61 to 0.87); moderate resistance, RD 0.50 (95% CI 0.40 to 0.60); high resistance, RD 0.39 (95% CI 0.24 to 0.54). For hut studies: low resistance, RD 0.56 (95% CI 0.43 to 0.68); moderate resistance, RD 0.39 (95% CI 0.16 to 0.61); high resistance, RD 0.35 (95% CI 0.27 to 0.43). However, with the exception of the moderate resistance category for tunnel tests, there was extremely high heterogeneity across studies in each resistance category (chi-squared test, p
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We therefore assessed the evidence that resistance is attenuating the effect of ITNs on entomological outcomes. We included laboratory and field studies of African malaria vectors that measured resistance at the time of the study and used World Health Organization-recommended impregnation regimens. We reported mosquito mortality, blood feeding, induced exophily (premature exit of mosquitoes from the hut), deterrence, time to 50% or 95% knock-down, and percentage knock-down at 60 min. Publications were searched from 1 January 1980 to 31 December 2013 using MEDLINE, Cochrane Central Register of Controlled Trials, Science Citation Index Expanded, Social Sciences Citation Index, African Index Medicus, and CAB Abstracts. We stratified studies into three levels of insecticide resistance, and ITNs were compared with untreated bed nets (UTNs) using the risk difference (RD). Heterogeneity was explored visually and statistically. Included were 36 laboratory and 24 field studies, reported in 25 records. Studies tested and reported resistance inconsistently. Based on the meta-analytic results, the difference in mosquito mortality risk for ITNs compared to UTNs was lower in higher resistance categories. However, mortality risk was significantly higher for ITNs compared to UTNs regardless of resistance. For cone tests: low resistance, risk difference (RD) 0.86 (95% CI 0.72 to 1.01); moderate resistance, RD 0.71 (95% CI 0.53 to 0.88); high resistance, RD 0.56 (95% CI 0.17 to 0.95). For tunnel tests: low resistance, RD 0.74 (95% CI 0.61 to 0.87); moderate resistance, RD 0.50 (95% CI 0.40 to 0.60); high resistance, RD 0.39 (95% CI 0.24 to 0.54). For hut studies: low resistance, RD 0.56 (95% CI 0.43 to 0.68); moderate resistance, RD 0.39 (95% CI 0.16 to 0.61); high resistance, RD 0.35 (95% CI 0.27 to 0.43). However, with the exception of the moderate resistance category for tunnel tests, there was extremely high heterogeneity across studies in each resistance category (chi-squared test, p&lt;0.00001, I² varied from 95% to 100%). This meta-analysis found that ITNs are more effective than UTNs regardless of resistance. There appears to be a relationship between resistance and the RD for mosquito mortality in laboratory and field studies. However, the substantive heterogeneity in the studies' results and design may mask the true relationship between resistance and the RD, and the results need to be interpreted with caution. Our analysis suggests the potential for cumulative meta-analysis in entomological trials, but further field research in this area will require specialists in the field to work together to improve the quality of trials, and to standardise designs, assessment, and reporting of both resistance and entomological outcomes.</description><identifier>ISSN: 1549-1676</identifier><identifier>ISSN: 1549-1277</identifier><identifier>EISSN: 1549-1676</identifier><identifier>DOI: 10.1371/journal.pmed.1001619</identifier><identifier>PMID: 24642791</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Africa ; Animals ; Biology and Life Sciences ; Culicidae - drug effects ; Health aspects ; Insecticide Resistance ; Insecticide-Treated Bednets - standards ; Insecticides ; Insecticides - pharmacology ; Malaria ; Malaria - prevention &amp; control ; Medicine and Health Sciences ; Mosquito Control - standards ; Mosquitoes ; Nets ; Netting ; Pyrethrins - pharmacology ; Pyrethroids ; Studies</subject><ispartof>PLoS medicine, 2014-03, Vol.11 (3), p.e1001619</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Strode et al 2014 Strode et al</rights><rights>2014 Strode et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Strode C, Donegan S, Garner P, Enayati AA, Hemingway J (2014) The Impact of Pyrethroid Resistance on the Efficacy of Insecticide-Treated Bed Nets against African Anopheline Mosquitoes: Systematic Review and Meta-Analysis. 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We therefore assessed the evidence that resistance is attenuating the effect of ITNs on entomological outcomes. We included laboratory and field studies of African malaria vectors that measured resistance at the time of the study and used World Health Organization-recommended impregnation regimens. We reported mosquito mortality, blood feeding, induced exophily (premature exit of mosquitoes from the hut), deterrence, time to 50% or 95% knock-down, and percentage knock-down at 60 min. Publications were searched from 1 January 1980 to 31 December 2013 using MEDLINE, Cochrane Central Register of Controlled Trials, Science Citation Index Expanded, Social Sciences Citation Index, African Index Medicus, and CAB Abstracts. We stratified studies into three levels of insecticide resistance, and ITNs were compared with untreated bed nets (UTNs) using the risk difference (RD). Heterogeneity was explored visually and statistically. Included were 36 laboratory and 24 field studies, reported in 25 records. Studies tested and reported resistance inconsistently. Based on the meta-analytic results, the difference in mosquito mortality risk for ITNs compared to UTNs was lower in higher resistance categories. However, mortality risk was significantly higher for ITNs compared to UTNs regardless of resistance. For cone tests: low resistance, risk difference (RD) 0.86 (95% CI 0.72 to 1.01); moderate resistance, RD 0.71 (95% CI 0.53 to 0.88); high resistance, RD 0.56 (95% CI 0.17 to 0.95). For tunnel tests: low resistance, RD 0.74 (95% CI 0.61 to 0.87); moderate resistance, RD 0.50 (95% CI 0.40 to 0.60); high resistance, RD 0.39 (95% CI 0.24 to 0.54). For hut studies: low resistance, RD 0.56 (95% CI 0.43 to 0.68); moderate resistance, RD 0.39 (95% CI 0.16 to 0.61); high resistance, RD 0.35 (95% CI 0.27 to 0.43). However, with the exception of the moderate resistance category for tunnel tests, there was extremely high heterogeneity across studies in each resistance category (chi-squared test, p&lt;0.00001, I² varied from 95% to 100%). This meta-analysis found that ITNs are more effective than UTNs regardless of resistance. There appears to be a relationship between resistance and the RD for mosquito mortality in laboratory and field studies. However, the substantive heterogeneity in the studies' results and design may mask the true relationship between resistance and the RD, and the results need to be interpreted with caution. Our analysis suggests the potential for cumulative meta-analysis in entomological trials, but further field research in this area will require specialists in the field to work together to improve the quality of trials, and to standardise designs, assessment, and reporting of both resistance and entomological outcomes.</description><subject>Africa</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Culicidae - drug effects</subject><subject>Health aspects</subject><subject>Insecticide Resistance</subject><subject>Insecticide-Treated Bednets - standards</subject><subject>Insecticides</subject><subject>Insecticides - pharmacology</subject><subject>Malaria</subject><subject>Malaria - prevention &amp; control</subject><subject>Medicine and Health Sciences</subject><subject>Mosquito Control - standards</subject><subject>Mosquitoes</subject><subject>Nets</subject><subject>Netting</subject><subject>Pyrethrins - pharmacology</subject><subject>Pyrethroids</subject><subject>Studies</subject><issn>1549-1676</issn><issn>1549-1277</issn><issn>1549-1676</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk9-KEzEUxgdR3HX1DUQDguDF1CSTyTReCGXxT2FxQVdvQyZz0qbMJLNJutqX8VlNbXdpYS-UEBKS3_cdzjmconhO8IRUDXm78uvgVD8ZB-gmBGPCiXhQnJKaiZLwhj88uJ8UT2JcYUwFFvhxcUIZZ7QR5LT4fbUEZIdR6YS8QeMmQFoGbzsUINqYlNOAvEMpY2CM1UpvtqB1EXSy2nZQpgAqQYfavB2kiNRC5f-EZiZkgUPK-XEJvXWABh-v1zZ5iO9Q3MQEg8ouOdiNhZ8Z7NAASZUqZ7bJ8Z8Wj4zqIzzbn2fF948frs4_lxeXn-bns4tSNxVPpaiFBtUaJgyuOirajrSUYqwZVQ2IjuIpNpRz3nIybQnngEXb1Izhum1p11Znxcud79j7KPeljZLUuXpkyhjNxHxHdF6t5BjsoMJGemXl3wcfFlKFnEoPUsCUEa5JK5qKaWCqqatGVawmmhrDptnr_T7aus3d0-BSUP2R6fGPs0u58DeyEvW0qkU2eLUzWKgczzrjM6YHG7WcVZzTiuOaZKq8h1qAg-zpHRibn4_4yT18Xh0MVt8reHMkyEyCX2mh1jHK-bev_8F--Xf28scx-_qAXYLq0zL6fp2sd_EYZDtQBx9jAHNXb4LldqJu2y63EyX3E5VlLw57dSe6HaHqDwnSHds</recordid><startdate>20140301</startdate><enddate>20140301</enddate><creator>Strode, Clare</creator><creator>Donegan, Sarah</creator><creator>Garner, Paul</creator><creator>Enayati, Ahmad Ali</creator><creator>Hemingway, Janet</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>5PM</scope><scope>DOA</scope><scope>CZK</scope></search><sort><creationdate>20140301</creationdate><title>The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis</title><author>Strode, Clare ; Donegan, Sarah ; Garner, Paul ; Enayati, Ahmad Ali ; Hemingway, Janet</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c736t-959ceabf49f03d29bd1b2200c42a7e9d2080f2666b618b166e09b754405bb2db3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Africa</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Culicidae - drug effects</topic><topic>Health aspects</topic><topic>Insecticide Resistance</topic><topic>Insecticide-Treated Bednets - standards</topic><topic>Insecticides</topic><topic>Insecticides - pharmacology</topic><topic>Malaria</topic><topic>Malaria - prevention &amp; control</topic><topic>Medicine and Health Sciences</topic><topic>Mosquito Control - standards</topic><topic>Mosquitoes</topic><topic>Nets</topic><topic>Netting</topic><topic>Pyrethrins - pharmacology</topic><topic>Pyrethroids</topic><topic>Studies</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Strode, Clare</creatorcontrib><creatorcontrib>Donegan, Sarah</creatorcontrib><creatorcontrib>Garner, Paul</creatorcontrib><creatorcontrib>Enayati, Ahmad Ali</creatorcontrib><creatorcontrib>Hemingway, Janet</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Medicine</collection><jtitle>PLoS medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Strode, Clare</au><au>Donegan, Sarah</au><au>Garner, Paul</au><au>Enayati, Ahmad Ali</au><au>Hemingway, Janet</au><au>Noor, Abdisalan Mohamed</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis</atitle><jtitle>PLoS medicine</jtitle><addtitle>PLoS Med</addtitle><date>2014-03-01</date><risdate>2014</risdate><volume>11</volume><issue>3</issue><spage>e1001619</spage><pages>e1001619-</pages><issn>1549-1676</issn><issn>1549-1277</issn><eissn>1549-1676</eissn><abstract>Pyrethroid insecticide-treated bed nets (ITNs) help contribute to reducing malaria deaths in Africa, but their efficacy is threatened by insecticide resistance in some malaria mosquito vectors. We therefore assessed the evidence that resistance is attenuating the effect of ITNs on entomological outcomes. We included laboratory and field studies of African malaria vectors that measured resistance at the time of the study and used World Health Organization-recommended impregnation regimens. We reported mosquito mortality, blood feeding, induced exophily (premature exit of mosquitoes from the hut), deterrence, time to 50% or 95% knock-down, and percentage knock-down at 60 min. Publications were searched from 1 January 1980 to 31 December 2013 using MEDLINE, Cochrane Central Register of Controlled Trials, Science Citation Index Expanded, Social Sciences Citation Index, African Index Medicus, and CAB Abstracts. We stratified studies into three levels of insecticide resistance, and ITNs were compared with untreated bed nets (UTNs) using the risk difference (RD). Heterogeneity was explored visually and statistically. Included were 36 laboratory and 24 field studies, reported in 25 records. Studies tested and reported resistance inconsistently. Based on the meta-analytic results, the difference in mosquito mortality risk for ITNs compared to UTNs was lower in higher resistance categories. However, mortality risk was significantly higher for ITNs compared to UTNs regardless of resistance. For cone tests: low resistance, risk difference (RD) 0.86 (95% CI 0.72 to 1.01); moderate resistance, RD 0.71 (95% CI 0.53 to 0.88); high resistance, RD 0.56 (95% CI 0.17 to 0.95). For tunnel tests: low resistance, RD 0.74 (95% CI 0.61 to 0.87); moderate resistance, RD 0.50 (95% CI 0.40 to 0.60); high resistance, RD 0.39 (95% CI 0.24 to 0.54). For hut studies: low resistance, RD 0.56 (95% CI 0.43 to 0.68); moderate resistance, RD 0.39 (95% CI 0.16 to 0.61); high resistance, RD 0.35 (95% CI 0.27 to 0.43). However, with the exception of the moderate resistance category for tunnel tests, there was extremely high heterogeneity across studies in each resistance category (chi-squared test, p&lt;0.00001, I² varied from 95% to 100%). This meta-analysis found that ITNs are more effective than UTNs regardless of resistance. There appears to be a relationship between resistance and the RD for mosquito mortality in laboratory and field studies. However, the substantive heterogeneity in the studies' results and design may mask the true relationship between resistance and the RD, and the results need to be interpreted with caution. Our analysis suggests the potential for cumulative meta-analysis in entomological trials, but further field research in this area will require specialists in the field to work together to improve the quality of trials, and to standardise designs, assessment, and reporting of both resistance and entomological outcomes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24642791</pmid><doi>10.1371/journal.pmed.1001619</doi><oa>free_for_read</oa></addata></record>
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subjects Africa
Animals
Biology and Life Sciences
Culicidae - drug effects
Health aspects
Insecticide Resistance
Insecticide-Treated Bednets - standards
Insecticides
Insecticides - pharmacology
Malaria
Malaria - prevention & control
Medicine and Health Sciences
Mosquito Control - standards
Mosquitoes
Nets
Netting
Pyrethrins - pharmacology
Pyrethroids
Studies
title The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis
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