The need for practical insecticide-resistance guidelines to effectively inform mosquito-borne disease control programs

Abstract

Monitoring local mosquito populations for insecticide resistance is critical for effective vector-borne disease control. However, widely used phenotypic assays, which are designed to monitor the emergence and spread of insecticide resistance (technical resistance), do not translate well to the efficacy of vector control products to suppress mosquito numbers in the field (practical resistance). This is because standard testing conditions such as environmental conditions, exposure dose, and type of substrate differ dramatically from those experienced by mosquitoes under field conditions. In addition, field mosquitoes have considerably different physiological characteristics such as age and blood-feeding status. Beyond this, indirect impacts of insecticide resistance and/or exposure on mosquito longevity, pathogen development, host-seeking behavior, and blood-feeding success impact disease transmission. Given the limited number of active ingredients currently available and the observed discordance between resistance and disease transmission, we conclude that additional testing guidelines are needed to determine practical resistance-the efficacy of vector control tools under relevant local conditions- in order to obtain programmatic impact.

Keywords: Aedes; Anopheles; Insecticide resistance; epidemiology; evolutionary biology; global health; policy; surveillance; vector control.

Figure 1.. Indirect effects of environment on insecticide resistance.

Environmental conditions such as climatic conditions (e.g., temperature and humidity), mosquito fitness (e.g., age, size, and feeding status), insecticide exposure time (e.g., fleeting contact vs extended exposure), and insecticide dose (depending on, e.g., time since application, washes, and insecticide half-life), which all vary over space and time, impact phenotypic resistance. To measure technical resistance, a particular phenotype (depending on the test used) is measured under standardized conditions. Variation is introduced by the researcher performing the test (e.g., variation in mosquito handling, test preparation, and mortality scoring). Phenotypic resistance translates indirectly to disease transmission: insecticide-resistance mechanisms and the insecticide itself impact the mosquitoes’ vectorial capacity (i.e., the ability of mosquito populations to transmit a specific pathogen from human to human) through host choice (e.g., frequency of human vs non-human biting), biting rate (i.e., frequency of taking a human blood meal), reproductive fitness (i.e., the ability of a mosquito to pass on her genes to subsequent generations, which is importantly impacted by survival, fertility, and ability to mate), and vector competence (i.e., the capacity of a mosquito to acquire, maintain, and transmit a parasite). In addition, phenotypic resistance indirectly translates to disease transmission through factors impacting the field efficacy of vector control tools because of aforementioned environmental conditions (i.e., practical resistance). The variation in use and deployment of the tool impacts the efficacy of the vector control tool itself, as well as vectorial capacity. Overall, these indirect effects could lead to poor correlation between standardized phenotypic tests and impact on disease transmission.