The Impact of Pyrethroid Resistance on the Efficacy of Insecticide-Treated Bed Nets against African Anopheline Mosquitoes: Systematic Review and Meta-Analysis
Background:
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.
Methods and Findings:
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<0.00001, I2 varied from 95% to 100%).
Conclusions:
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.
Please see later in the article for the Editors' Summary
Vyšlo v časopise:
The Impact of Pyrethroid Resistance on the Efficacy of Insecticide-Treated Bed Nets against African Anopheline Mosquitoes: Systematic Review and Meta-Analysis. PLoS Med 11(3): e32767. doi:10.1371/journal.pmed.1001619
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pmed.1001619
Souhrn
Background:
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.
Methods and Findings:
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<0.00001, I2 varied from 95% to 100%).
Conclusions:
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.
Please see later in the article for the Editors' Summary
Zdroje
1. World Health Organization (2011) World malaria report 2011. Geneva: World Health Organization.
2. LengelerC (2004) Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev 2004: CD000363.
3. JonesCM, SanouA, GuelbeogoWM, SagnonN, JohnsonPC, et al. (2012) Aging partially restores the efficacy of malaria vector control in insecticide-resistant populations of Anopheles gambiae s.l. from Burkina Faso. Malar J 11: 24.
4. OkiaM, NdyomugyenyiR, KirundaJ, ByaruhangaA, AdibakuS, et al. (2013) Bioefficacy of long-lasting insecticidal nets against pyrethroid-resistant populations of Anopheles gambiae s.s. from different malaria transmission zones in Uganda. Parasit Vectors 6: 130.
5. World Health Organization (2010) World malaria report 2010. Geneva: World Health Organization.
6. OkumuFO, ChipwazaB, MadumlaEP, MbeyelaE, LingambaG, et al. (2012) Implications of bio-efficacy and persistence of insecticides when indoor residual spraying and long-lasting insecticide nets are combined for malaria prevention. Malar J 11: 378.
7. BrietOJ, PennyMA, HardyD, AwololaTS, Van BortelW, 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: 77.
8. HougardJM, DuchonS, DarrietF, ZaimM, RogierC, et al. (2003) Comparative performances, under laboratory conditions, of seven pyrethroid insecticides used for impregnation of mosquito nets. Bull World Health Organ 81: 324–333.
9. OkumuFO, MbeyelaE, LingambaG, MooreJ, NtamatungiroAJ, et al. (2013) Comparative field evaluation of combinations of long-lasting insecticide treated nets and indoor residual spraying, relative to either method alone, for malaria prevention in an area where the main vector is Anopheles arabiensis. Parasit Vectors 6: 46.
10. Darriet F, Robert V, Tho Vien N, Carnevale P (1984) Evaluation of the efficacy of permethrin-impregnated intact and perforated mosquito nets against vectors of malaria. WHO/VBC/84.899. Geneva: World Health Organization.
11. RansonH, N'GuessanR, LinesJ, MoirouxN, NkuniZ, et al. (2011) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 91–98.
12. TrapeJF, TallA, DiagneN, NdiathO, LyAB, et al. (2011) Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis 11: 925–932.
13. World Health Organization (2012) Global plan for insecticide resistance management in malaria vectors. Geneva: World Health Organization.
14. Martinez-TorresD, ChandreF, WilliamsonMS, DarrietF, BergeJB, et al. (1998) Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol 7: 179–184.
15. RansonH, JensenB, VululeJM, WangX, HemingwayJ, et al. (2000) 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 9: 491–497.
16. HemingwayJ, HawkesNJ, McCarrollL, RansonH (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34: 653–665.
17. DjouakaRF, BakareAA, CoulibalyON, AkogbetoMC, RansonH, et al. (2008) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. BMC Genomics 9: 538.
18. AwololaTS, OduolaOA, StrodeC, KoekemoerLL, BrookeB, et al. (2009) Evidence of multiple pyrethroid resistance mechanisms in the malaria vector Anopheles gambiae sensu stricto from Nigeria. Trans R Soc Trop Med Hyg 103: 1139–1145.
19. MullerP, WarrE, StevensonBJ, PignatelliPM, MorganJC, et al. (2008) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet 4: e1000286.
20. MitchellSN, StevensonBJ, MullerP, WildingCS, Egyir-YawsonA, et al. (2012) Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci U S A 109: 6147–6152.
21. WoodO, HanrahanS, CoetzeeM, KoekemoerL, BrookeB (2010) Cuticle thickening associated with pyrethroid resistance in the major malaria vector Anopheles funestus. Parasit Vectors 3: 67.
22. NdiathMO, SougoufaraS, GayeA, MazenotC, KonateL, et al. (2012) Resistance to DDT and pyrethroids and increased kdr mutation frequency in An. gambiae after the implementation of permethrin-treated nets in Senegal. PLoS ONE 7: e31943.
23. NorrisLC, NorrisDE (2011) Insecticide resistance in Culex quinquefasciatus mosquitoes after the introduction of insecticide-treated bed nets in Macha, Zambia. J Vector Ecol 36: 411–420.
24. RansonH, AbdallahH, BadoloA, GuelbeogoWM, Kerah-HinzoumbeC, et al. (2009) Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J 8: 299.
25. World Health Organization (2005) Guidelines for laboratory and field testing of long-lasting insecticidal mosquito nets. WHO/CDS/WHOPES/GCDPP/2005.11. Geneva: World Health Organization.
26. World Health Organization (2013) Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization.
27. ThorlundK, ImbergerG, JohnstonBC, WalshM, AwadT, et al. (2012) Evolution of heterogeneity (I2) estimates and their 95% confidence intervals in large meta-analyses. PLoS ONE 7: e39471.
28. AsidiAN, N'GuessanR, KoffiAA, CurtisCF, HougardJM, 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.
29. ChandreF, DarrietF, DuchonS, FinotL, ManguinS, et al. (2000) Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae. Med Vet Entomol 14: 81–88.
30. CorbelV, ChandreF, BrenguesC, AkogbetoM, LardeuxF, et al. (2004) Dosage-dependent effects of permethrin-treated nets on the behaviour of Anopheles gambiae and the selection of pyrethroid resistance. Malar J 3: 22.
31. CorbelV, ChabiJ, DabireRK, EtangJ, NwaneP, 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.
32. DarrietF, GuilletP, N'GuessanR, DoannioJM, KoffiA, et al. (1998) [Impact of resistance of Anopheles gambiae s.s. to permethrin and deltamethrin on the efficacy of impregnated mosquito nets.]. Med Trop (Mars) 58: 349–354.
33. DarrietF, N'GuessanR, KoffiAA, KonanL, DoannioJMC, et al. (2000) Impact of the resistance to pyrethroids on the efficacy of impregnated bednets used as a means of prevention against malaria: results of the evaluation carried out with deltamethrin SC in experimental huts. Bull Soc Pathol Exot 93: 131–134.
34. DjenontinA, ChandreF, DabireKR, ChabiJ, N'GuessanR, et al. (2010) Indoor use of plastic sheeting impregnated with carbamate combined with long-lasting insecticidal mosquito nets for the control of pyrethroid-resistant malaria vectors. Am J Trop Med Hyg 83: 266–270.
35. FanelloC, KolaczinskiJH, ConwayDJ, CarnevaleP, CurtisCF (1999) The kdr pyrethroid resistance gene in Anopheles gambiae: tests of non-pyrethroid insecticides and a new detection method for the gene. Parassitologia 41: 323–326.
36. MalimaRC, MagesaSM, TunguPK, MwingiraV, MagogoFS, et al. (2008) An experimental hut evaluation of Olyset (R) nets against anopheline mosquitoes after seven years use in Tanzanian villages. Malaria Journal 7: 38.
37. MalimaRC, OxboroughRM, TunguPK, MaxwellC, LyimoI, et al. (2009) Behavioural and insecticidal effects of organophosphate-, carbamate- and pyrethroid-treated mosquito nets against African malaria vectors. Med Vet Entomol 23: 317–325.
38. N'GuessanR, BokoP, OdjoA, AkogbetoM, YatesA, et al. (2007) Chlorfenapyr: a pyrrole insecticide for the control of pyrethroid or DDT resistant Anopheles gambiae (Diptera: Culicidae) mosquitoes. Acta Trop 102: 69–78.
39. NguforC, N'GuessanR, BokoP, OdjoA, VigninouE, 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: 343.
40. OxboroughRM, WeirV, IrishS, KaurH, N'GuessanR, et al. (2009) Is K-O Tab 1-2-3((R)) long lasting on non-polyester mosquito nets? Acta Trop 112: 49–53.
41. TunguP, MagesaS, MaxwellC, MalimaR, MasueD, 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: 21.
42. KoudouBG, KoffiAA, MaloneD, HemingwayJ (2011) Efficacy of PermaNet(R) 2.0 and PermaNet(R) 3.0 against insecticide-resistant Anopheles gambiae in experimental huts in Cote d'Ivoire. Malar J 10: 172.
43. EtangJ, ChandreF, GuilletP, MangaL (2004) Reduced bio-efficacy of permethrin EC impregnated bednets against an Anopheles gambiae strain with oxidase-based pyrethroid tolerance. Malar J 3: 46.
44. HodjatiMH, CurtisCF (1999) Evaluation of the effect of mosquito age and prior exposure to insecticide on pyrethroid tolerance in Anopheles mosquitoes (Diptera: Culicidae). Bull Entomol Res 89: 329–337.
45. GimnigJE, LindbladeKA, MountDL, AtieliFK, CrawfordS, et al. (2005) Laboratory wash resistance of long-lasting insecticidal nets. Trop Med Int Health 10: 1022–1029.
46. MahamaT, DesireeEJ, PierreC, FabriceC (2007) Effectiveness of permanet in Cote d'Ivoire rural areas and residual activity on a knockdown-resistant strain of Anopheles gambiae. J Med Entomol 44: 498–502.
47. FaneM, CisseO, TraoreCS, SabatierP (2012) Anopheles gambiae resistance to pyrethroid-treated nets in cotton versus rice areas in Mali. Acta Trop 122: 1–6.
48. WinklerMS, TchicayaE, KoudouBG, DonzeJ, NsanzabanaC, et al. (2012) Efficacy of ICON(R) Maxx in the laboratory and against insecticide-resistant Anopheles gambiae in central Cote d'Ivoire. Malar J 11: 167.
49. OxboroughRM, KitauJ, MatowoJ, FestonE, MndemeR, et al. (2013) ITN mixtures of chlorfenapyr (pyrrole) and alphacypermethrin (pyrethroid) for control of pyrethroid resistant Anopheles arabiensis and Culex quinquefasciatus. PLoS ONE 8: e55781.
50. N'GuessanR, CorbelV, AkogbetoM, RowlandM (2007) Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis 13: 199–206.
51. World Health Organization (1998) Test procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticide on treated surfaces. Geneva: World Health Organization.
52. BrookeBD (2008) kdr: can a single mutation produce an entire insecticide resistance phenotype? Trans R Soc Trop Med Hyg 102: 524–525.
53. DonnellyMJ, CorbelV, WeetmanD, WildingCS, WilliamsonMS, et al. (2009) Does kdr genotype predict insecticide-resistance phenotype in mosquitoes? Trends Parasitol 25: 213–219.
54. IrvingH, RiveronJM, IbrahimSS, LoboNF, WondjiCS (2012) Positional cloning of rp2 QTL associates the P450 genes CYP6Z1, CYP6Z3 and CYP6M7 with pyrethroid resistance in the malaria vector Anopheles funestus. Heredity (Edinb) 109: 383–392.
55. StevensonBJ, PignatelliP, NikouD, PaineMJ (2012) Pinpointing P450s associated with pyrethroid metabolism in the dengue vector, Aedes aegypti: developing new tools to combat insecticide resistance. PLoS Negl Trop Dis 6: e1595.
56. StevensonBJ, BibbyJ, PignatelliP, MuangnoicharoenS, O'NeillPM, et al. (2011) Cytochrome P450 6M2 from the malaria vector Anopheles gambiae metabolizes pyrethroids: sequential metabolism of deltamethrin revealed. Insect Biochem Mol Biol 41: 492–502.
57. HargreavesK, KoekemoerLL, BrookeBD, HuntRH, MthembuJ, et al. (2000) Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 14: 181–189.
58. WondjiCS, IrvingH, MorganJ, LoboNF, CollinsFH, et al. (2009) Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Res 19: 452–459.
59. AmenyaDA, NaguranR, LoTC, RansonH, SpillingsBL, et al. (2008) Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles Funestus, resistant to pyrethroids. Insect Mol Biol 17: 19–25.
60. BonizzoniM, AfraneY, BaliraineFN, AmenyaDA, GithekoAK, et al. (2009) Genetic structure of Plasmodium falciparum populations between lowland and highland sites and antimalarial drug resistance in Western Kenya. Infect Genet Evol 9: 806–812.
61. DabireRK, DiabateA, BaldetT, Pare-ToeL, GuiguemdeRT, et al. (2006) Personal protection of long lasting insecticide-treated nets in areas of Anopheles gambiae s.s. resistance to pyrethroids. Malar J 5: 12.
62. GithekoAK, AdungoNI, KaranjaDM, HawleyWA, VululeJM, et al. (1996) Some observations on the biting behavior of Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus and their implications for malaria control. Exp Parasitol 82: 306–315.
63. World Health Organization (2007) Insecticide-treated nets: a WHO position statement. Geneva: World Health Organization.
64. IoanndisJP, GreenlandS, HlatkyMA, KhouryMJ, MacleodMR, et al. (2014) Increasing value and reducing waste in research design, conduct, and analysis. Lancet 383: 166–175 doi:10.1016/S0140-6736(13)62227-8
Štítky
Interné lekárstvoČlánok vyšiel v časopise
PLOS Medicine
2014 Číslo 3
- Statinová intolerance
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Co dělat při intoleranci statinů?
- Pleiotropní účinky statinů na kardiovaskulární systém
- DESATORO PRE PRAX: Aktuálne odporúčanie ESPEN pre nutričný manažment u pacientov s COVID-19
Najčítanejšie v tomto čísle
- and Water, Sanitation, and Hygiene: A Committed Relationship
- Representation and Misrepresentation of Scientific Evidence in Contemporary Tobacco Regulation: A Review of Tobacco Industry Submissions to the UK Government Consultation on Standardised Packaging
- The Role of Viral Introductions in Sustaining Community-Based HIV Epidemics in Rural Uganda: Evidence from Spatial Clustering, Phylogenetics, and Egocentric Transmission Models
- How Can Journals Respond to Threats of Libel Litigation?