Fine-scale spatial and temporal heterogeneities in insecticide resistance profiles of the malaria vector, Anopheles arabiensis in rural south-eastern Tanzania

Abstract

Background: Programmatic monitoring of insecticide resistance in disease vectors is mostly done on a large scale, often focusing on differences between districts, regions or countries. However, local heterogeneities in residual malaria transmission imply the need for finer-scale data. This study reports small-scale variations of insecticide susceptibility in Anopheles arabiensis between three neighbouring villages across two seasons in Tanzania, where insecticidal bed nets are extensively used, but malaria transmission persists. Methods: WHO insecticide susceptibility assays were conducted on female and male An. arabiensis from three proximal villages, Minepa, Lupiro, and Mavimba, during dry (June-December 2015) and wet (January-May 2016) seasons. Adults emerging from wild-collected larvae were exposed to 0.05% lambda-cyhalothrin, 0.05% deltamethrin, 0.75% permethrin, 4% DDT, 4% dieldrin, 0.1% bendiocarb, 0.1% propoxur, 0.25% pirimiphos-methyl and 5% malathion. A hydrolysis probe assay was used to screen for L1014F ( kdr-w) and L1014S ( kdr-e) mutations in specimens resistant to DDT or pyrethroids. Synergist assays using piperonly butoxide (PBO) and triphenol phosphate (TPP) were done to assess pyrethroid and bendiocarb resistance phenotypes. Results: There were clear seasonal and spatial fluctuations in phenotypic resistance status in An. arabiensis to pyrethroids, DDT and bendiocarb. Pre-exposure to PBO and TPP, resulted in lower knockdown rates and higher mortalities against pyrethroids and bendiocarb, compared to tests without the synergists. Neither L1014F nor L1014S mutations were detected. Conclusions: This study confirmed the presence of pyrethroid resistance in An. arabiensis and showed small-scale differences in resistance levels between the villages, and between seasons. Substantial, though incomplete, reversal of pyrethroid and bendiocarb resistance following pre-exposure to PBO and TPP, and absence of kdr alleles suggest involvement of P450 monooxygenases and esterases in the resistant phenotypes. We recommend, for effective resistance management, further bioassays to quantify the strength of resistance, and both biochemical and molecular analysis to elucidate specific enzymes responsible in resistance.

Opinions of key stakeholders on alternative interventions for malaria control and elimination in Tanzania

“…A significant slowdown in the decline of malaria cases and deaths has been observed over the past decade; between 2010 and 2018, the rate of malaria cases and deaths have only declined by 22% and 30%, respectively [2]. Mosquito resistance to insecticides used in indoor residual spraying and bed nets is now widely documented worldwide [4,5]. An increasing disposition of malaria vector to bite during the early-evening hours and the early morning, and to do so outdoor, is also well documented [6,7], threatening the success of the major interventions for malaria control.…”

Anopheles funestus mosquitoes from rural south-eastern Tanzania may have stronger resistance to pyrethroids than the other malaria vector, Anopheles arabiensis

“…As demonstrated by Matowo et al for both An. arabiensis and Culex mosquitoes [45,58], there were signs of ne-scale spatial variations in insecticide resistance. For example, An.…”

Patterns of pesticides usage in agriculture in rural Tanzania call for integrating agricultural and public health practices in managing insecticide-resistance in malaria vectors

“…Anopheles funestus s.snd An. arabiensis are the predominant malaria vectors [27,28]. Additionally, non-malaria vectors, such as Culex and Mansonia, constitute biting nuisances [33,34].…”

“…Additionally, non-malaria vectors, such as Culex and Mansonia, constitute biting nuisances [33,34]. Though pyrethroid-based LLINs are the main malaria intervention [35], mosquito populations are resistant to pyrethroids, bendiocarb (carbamates), and DDT [27,28,34].…”

“…The purpose of this study was to explore agricultural pesticides, pesticide usage practices, awareness, and management practices among retailers and farming communities from a rural malaria endemic area in south-eastern Tanzania, where mosquito vectors are resistant to public health insecticides [27,28]. The ndings are expected to guide practical recommendations for collaboration between agriculture and public health sectors in insecticide resistance management in mosquito vectors and disease control.…”