Association of Reduced Long-Lasting Insecticidal Net Efficacy and Pyrethroid Insecticide Resistance With Overexpression of CYP6P4, CYP6P3, and CYP6Z1 in Populations of Anopheles coluzzii From Southeast Côte d'Ivoire.
Anopheles coluzzii
CYP6P3
CYP6P4
CYP6Z1
Plasmodium falciparum
Côte d’Ivoire
PBO
chlorfenapyr
clothianidin
insecticide resistance
long-lasting insecticidal nets
Journal
The Journal of infectious diseases
ISSN: 1537-6613
Titre abrégé: J Infect Dis
Pays: United States
ID NLM: 0413675
Informations de publication
Date de publication:
19 04 2022
19 04 2022
Historique:
received:
10
09
2020
accepted:
02
11
2020
pubmed:
12
11
2020
medline:
21
4
2022
entrez:
11
11
2020
Statut:
ppublish
Résumé
Resistance to major public health insecticides in Côte d'Ivoire has intensified and now threatens the long-term effectiveness of malaria vector control interventions. This study evaluated the bioefficacy of conventional and next-generation long-lasting insecticidal nets (LLINs), determined resistance profiles, and characterized molecular and metabolic mechanisms in wild Anopheles coluzzii from Southeast Côte d'Ivoire in 2019. Phenotypic resistance was intense: >25% of mosquitoes survived exposure to 10 times the doses of pyrethroids required to kill susceptible populations. Similarly, the 24-hour mortality rate with deltamethrin-only LLINs was very low and not significantly different from that with an untreated net. Sublethal pyrethroid exposure did not induce significant delayed vector mortality effects 72 hours later. In contrast, LLINs containing the synergist piperonyl butoxide, or new insecticides clothianidin and chlorfenapyr, were highly toxic to A. coluzzii. Pyrethroid-susceptible A. coluzzii were significantly more likely to be infected with malaria, compared with those that survived insecticidal exposure. Pyrethroid resistance was associated with significant overexpression of CYP6P4, CYP6P3, and CYP6Z1. Study findings raise concerns regarding the operational failure of standard LLINs and support the urgent deployment of vector control interventions incorporating piperonyl butoxide, chlorfenapyr, or clothianidin in areas of high resistance intensity in Côte d'Ivoire.
Sections du résumé
BACKGROUND
Resistance to major public health insecticides in Côte d'Ivoire has intensified and now threatens the long-term effectiveness of malaria vector control interventions.
METHODS
This study evaluated the bioefficacy of conventional and next-generation long-lasting insecticidal nets (LLINs), determined resistance profiles, and characterized molecular and metabolic mechanisms in wild Anopheles coluzzii from Southeast Côte d'Ivoire in 2019.
RESULTS
Phenotypic resistance was intense: >25% of mosquitoes survived exposure to 10 times the doses of pyrethroids required to kill susceptible populations. Similarly, the 24-hour mortality rate with deltamethrin-only LLINs was very low and not significantly different from that with an untreated net. Sublethal pyrethroid exposure did not induce significant delayed vector mortality effects 72 hours later. In contrast, LLINs containing the synergist piperonyl butoxide, or new insecticides clothianidin and chlorfenapyr, were highly toxic to A. coluzzii. Pyrethroid-susceptible A. coluzzii were significantly more likely to be infected with malaria, compared with those that survived insecticidal exposure. Pyrethroid resistance was associated with significant overexpression of CYP6P4, CYP6P3, and CYP6Z1.
CONCLUSIONS
Study findings raise concerns regarding the operational failure of standard LLINs and support the urgent deployment of vector control interventions incorporating piperonyl butoxide, chlorfenapyr, or clothianidin in areas of high resistance intensity in Côte d'Ivoire.
Identifiants
pubmed: 33175129
pii: 5973957
doi: 10.1093/infdis/jiaa699
pmc: PMC9016462
doi:
Substances chimiques
Insecticides
0
Pyrethrins
0
Piperonyl Butoxide
LWK91TU9AH
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1424-1434Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 101285/Z/13/Z
Pays : United Kingdom
Informations de copyright
© The Author(s) 2020. Published by Oxford University Press for the Infectious Diseases Society of America.
Références
Parasit Vectors. 2020 Jan 10;13(1):17
pubmed: 31924276
Curr Opin Insect Sci. 2020 Jun;39:42-49
pubmed: 32109860
Wellcome Open Res. 2017 Aug 24;2:71
pubmed: 29018842
Sante. 1994 Mar-Apr;4(2):95-9
pubmed: 8186931
Emerg Infect Dis. 2012 Sep;18(9):1508-11
pubmed: 22932478
Parasit Vectors. 2016 Feb 24;9:100
pubmed: 26911550
Biomed Res Int. 2018 Oct 08;2018:2874160
pubmed: 30402467
Insect Biochem Mol Biol. 2016 Nov;78:50-57
pubmed: 27613592
Malar J. 2011 Oct 04;10:288
pubmed: 21970433
Infect Dis Poverty. 2019 Jul 15;8(1):64
pubmed: 31307509
Lancet Infect Dis. 2018 Jun;18(6):640-649
pubmed: 29650424
Sci Rep. 2019 Jun 20;9(1):8846
pubmed: 31222175
Med Vet Entomol. 2003 Mar;17(1):19-25
pubmed: 12680920
Insect Mol Biol. 2004 Feb;13(1):1-7
pubmed: 14728661
Evol Appl. 2017 Dec 04;11(4):431-441
pubmed: 29636797
Parasit Vectors. 2014 Nov 28;7:500
pubmed: 25429888
Parasit Vectors. 2018 Jan 8;11(1):19
pubmed: 29310704
Behav Ecol. 2010 Sep;21(5):1087-1092
pubmed: 22476108
PLoS One. 2013;8(1):e54820
pubmed: 23349974
Nature. 2014 Dec 18;516(7531):387-90
pubmed: 25470038
Malar J. 2019 Aug 1;18(1):264
pubmed: 31370898
Malar J. 2020 Dec 9;19(1):454
pubmed: 33298071
PLoS One. 2019 Apr 11;14(4):e0215074
pubmed: 30973948
PLoS Genet. 2014 Mar 20;10(3):e1004236
pubmed: 24651294
Ann Soc Belg Med Trop. 1993 Dec;73(4):291-4
pubmed: 8129474
Proc Natl Acad Sci U S A. 2012 Apr 24;109(17):6614-9
pubmed: 22493253
Nature. 2017 Dec 7;552(7683):96-100
pubmed: 29186111
Malar J. 2016 Aug 24;15(1):426
pubmed: 27553959
PLoS Genet. 2008 Nov;4(11):e1000286
pubmed: 19043575
Evol Appl. 2015 Apr;8(4):326-45
pubmed: 25926878
Emerg Infect Dis. 2014 Oct;20(10):1691-6
pubmed: 25279965
Malar J. 2019 Jul 17;18(1):244
pubmed: 31315630
Parasit Vectors. 2012 Apr 02;5:68
pubmed: 22472088
Malar J. 2012 Jan 23;11:24
pubmed: 22269002
Parasite. 2018;25:42
pubmed: 30088473
Malar J. 2020 Jan 15;19(1):24
pubmed: 31941502
Parasit Vectors. 2019 Jan 6;12(1):9
pubmed: 30612581
Parasit Vectors. 2019 Nov 15;12(1):544
pubmed: 31730481
Lancet. 2018 Apr 21;391(10130):1551-1552
pubmed: 29655495
Parasit Vectors. 2018 Oct 22;11(1):550
pubmed: 30348209
Bull World Health Organ. 1999;77(3):230-4
pubmed: 10212513
Proc Natl Acad Sci U S A. 2016 Aug 9;113(32):8975-80
pubmed: 27402740
Malar J. 2008 Aug 25;7:163
pubmed: 18724871