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Molecular surveillance of insecticide resistance in Phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in India

Molecular surveillance of resistance is an increasingly important part of vector borne disease control programmes that utilise insecticides. The visceral leishmaniasis (VL) elimination programme in India uses indoor residual spraying (IRS) with the pyrethroid, alpha-cypermethrin to control Phlebotom...

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Autores principales: Reid, Emma, Deb, Rinki Michelle, Ali, Asgar, Singh, Rudra Pratap, Mishra, Prabhas Kumar, Shepherd, Josephine, Singh, Anand Mohan, Bharti, Aakanksha, Singh, Chandramani, Sharma, Sadhana, Coleman, Michael, Weetman, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10659200/
https://www.ncbi.nlm.nih.gov/pubmed/37939123
http://dx.doi.org/10.1371/journal.pntd.0011734
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author Reid, Emma
Deb, Rinki Michelle
Ali, Asgar
Singh, Rudra Pratap
Mishra, Prabhas Kumar
Shepherd, Josephine
Singh, Anand Mohan
Bharti, Aakanksha
Singh, Chandramani
Sharma, Sadhana
Coleman, Michael
Weetman, David
author_facet Reid, Emma
Deb, Rinki Michelle
Ali, Asgar
Singh, Rudra Pratap
Mishra, Prabhas Kumar
Shepherd, Josephine
Singh, Anand Mohan
Bharti, Aakanksha
Singh, Chandramani
Sharma, Sadhana
Coleman, Michael
Weetman, David
author_sort Reid, Emma
collection PubMed
description Molecular surveillance of resistance is an increasingly important part of vector borne disease control programmes that utilise insecticides. The visceral leishmaniasis (VL) elimination programme in India uses indoor residual spraying (IRS) with the pyrethroid, alpha-cypermethrin to control Phlebotomus argentipes the vector of Leishmania donovani, the causative agent of VL. Prior long-term use of DDT may have selected for knockdown resistance (kdr) mutants (1014F and S) at the shared DDT and pyrethroid target site, which are common in India and can also cause pyrethroid cross-resistance. We monitored the frequency of these marker mutations over five years from 2017–2021 in sentinel sites in eight districts of north-eastern India covered by IRS. Frequencies varied markedly among the districts, though finer scale variation, among villages within districts, was limited. A pronounced and highly significant increase in resistance-associated genotypes occurred between 2017 and 2018, but with relative stability thereafter, and some reversion toward more susceptible genotypes in 2021. Analyses linked IRS with mutant frequencies suggesting an advantage to more resistant genotypes, especially when pyrethroid was under-sprayed in IRS. However, this advantage did not translate into sustained allele frequency changes over the study period, potentially because of a relatively greater net advantage under field conditions for a wild-type/mutant genotype than projected from laboratory studies and/or high costs of the most resistant genotype. Further work is required to improve calibration of each 1014 genotype with resistance, preferably using operationally relevant measures. The lack of change in resistance mechanism over the span of the study period, coupled with available bioassay data suggesting susceptibility, suggests that resistance has yet to emerge despite intensive IRS. Nevertheless, the advantage of resistance-associated genotypes with IRS and under spraying, suggest that measures to continue monitoring and improvement of spray quality are vital, and consideration of future alternatives to pyrethroids for IRS would be advisable.
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spelling pubmed-106592002023-11-08 Molecular surveillance of insecticide resistance in Phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in India Reid, Emma Deb, Rinki Michelle Ali, Asgar Singh, Rudra Pratap Mishra, Prabhas Kumar Shepherd, Josephine Singh, Anand Mohan Bharti, Aakanksha Singh, Chandramani Sharma, Sadhana Coleman, Michael Weetman, David PLoS Negl Trop Dis Research Article Molecular surveillance of resistance is an increasingly important part of vector borne disease control programmes that utilise insecticides. The visceral leishmaniasis (VL) elimination programme in India uses indoor residual spraying (IRS) with the pyrethroid, alpha-cypermethrin to control Phlebotomus argentipes the vector of Leishmania donovani, the causative agent of VL. Prior long-term use of DDT may have selected for knockdown resistance (kdr) mutants (1014F and S) at the shared DDT and pyrethroid target site, which are common in India and can also cause pyrethroid cross-resistance. We monitored the frequency of these marker mutations over five years from 2017–2021 in sentinel sites in eight districts of north-eastern India covered by IRS. Frequencies varied markedly among the districts, though finer scale variation, among villages within districts, was limited. A pronounced and highly significant increase in resistance-associated genotypes occurred between 2017 and 2018, but with relative stability thereafter, and some reversion toward more susceptible genotypes in 2021. Analyses linked IRS with mutant frequencies suggesting an advantage to more resistant genotypes, especially when pyrethroid was under-sprayed in IRS. However, this advantage did not translate into sustained allele frequency changes over the study period, potentially because of a relatively greater net advantage under field conditions for a wild-type/mutant genotype than projected from laboratory studies and/or high costs of the most resistant genotype. Further work is required to improve calibration of each 1014 genotype with resistance, preferably using operationally relevant measures. The lack of change in resistance mechanism over the span of the study period, coupled with available bioassay data suggesting susceptibility, suggests that resistance has yet to emerge despite intensive IRS. Nevertheless, the advantage of resistance-associated genotypes with IRS and under spraying, suggest that measures to continue monitoring and improvement of spray quality are vital, and consideration of future alternatives to pyrethroids for IRS would be advisable. Public Library of Science 2023-11-08 /pmc/articles/PMC10659200/ /pubmed/37939123 http://dx.doi.org/10.1371/journal.pntd.0011734 Text en © 2023 Reid et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Reid, Emma
Deb, Rinki Michelle
Ali, Asgar
Singh, Rudra Pratap
Mishra, Prabhas Kumar
Shepherd, Josephine
Singh, Anand Mohan
Bharti, Aakanksha
Singh, Chandramani
Sharma, Sadhana
Coleman, Michael
Weetman, David
Molecular surveillance of insecticide resistance in Phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in India
title Molecular surveillance of insecticide resistance in Phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in India
title_full Molecular surveillance of insecticide resistance in Phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in India
title_fullStr Molecular surveillance of insecticide resistance in Phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in India
title_full_unstemmed Molecular surveillance of insecticide resistance in Phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in India
title_short Molecular surveillance of insecticide resistance in Phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in India
title_sort molecular surveillance of insecticide resistance in phlebotomus argentipes targeted by indoor residual spraying for visceral leishmaniasis elimination in india
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10659200/
https://www.ncbi.nlm.nih.gov/pubmed/37939123
http://dx.doi.org/10.1371/journal.pntd.0011734
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