Kai Blore1,2*
Rebecca Baldwin2
Christopher D. Batich3
Phillip Koehler2Roberto Pereira2
Cameron J. Jack2Whitney A. Qualls1Rui-De Xue1- 1Anastasia Mosquito Control District, St. Augustine, FL, United States
- 2Department of Entomology and Nematology, University of Florida, Gainesville, FL, United States
- 3Department of Materials Science and Engineering, University of Florida, Gainesville, FL, United States
Presently, there is a need to develop effective and novel modes of control for mosquitoes, which remain a key driver of infectious disease transmission throughout the world. Control methods for these vectors have historically relied on a limited number of active ingredients (AIs) that have not experienced significant change in usage since the mid-20th century. The resulting development of widespread insecticide resistance has consequently increased the risk for future vector-borne disease outbreaks. Recently, metal nanoparticles have been explored for potential use in mosquito control due to their demonstrated toxicity against mosquitoes at all life stages. However, the majority of studies to date have focused on the larvicidal efficacy of metal nanoparticles with few studies examining their adulticidal potential. In this review, we analyze the current literature on green synthesized metal nanoparticles and their effect on adult mosquitoes.
Introduction
Vector-borne disease remains a leading cause of death worldwide despite sustained eradication programs across Africa, Asia, and South America. Malaria and dengue have been identified as threats to global health by WHO accounting for a global 230 million and 96 million symptomatic cases in 2019 respectively (1). Unfortunately, vector-borne disease will continue to be of public health importance due to the confluence of changing climate, globalization and urbanization which together are likely to increase rates of transmission. Rising temperatures, in particular are predicted to expand the geographic range of many vector species, increase the transmission season length, and provide shorter incubation period for vector species and their associated pathogens (2). This rising incidence will largely be driven by mosquito-borne diseases (3) such as yellow fever, dengue, Zika, chikungunya, West Nile, eastern equine encephalitis and St. Louis encephalitis viruses for which most have no available vaccines. As such, mosquito control remains the most effective preventative strategy.
Current mosquito control strategies employ a combination of source reduction, larviciding and adulticiding. Of these three options, adult insecticides have historically provided control operations with an effective means to quickly target and suppress mosquito population outbreaks with ultra-low volume (ULV) spraying being the preferred delivery method (4). Unfortunately, sustained use and reliance on a small group of chemical classes of insecticides (i.e. pyrethroids, organophosphates and carbamates) has led to the development of widespread insecticide resistance (5–8). Continued use of these same active ingredients (AIs) overtime will lead to diminished effectiveness (9) and may lead to the resurgence of mosquito-borne diseases (10).
To mitigate further development of resistance and retain insecticide efficacy, new AIs and formulations are necessary. However, development can be prohibitively expensive, due in part to strict regulatory requirements encompassing toxicological and safety studies that promote more selective and less persistent insecticides (11). Registration of a new chemical AI costs an estimated 250 million USD and can take fifteen years of research and development to complete (12–14). This gap in effective control tools and insecticide resistance has led to increasing interest in alternative sources of insecticides.
Nanotechnology has grown as a potential tool in insecticide application. Metal nanoparticles, in particular, are increasingly being incorporated into scientific and medical applications for the purposes of catalysis, imaging, diagnostics, drug delivery and pest management (15–20). Due to their wide array of applications, nanoparticles are currently one of the most active areas of research in the material sciences, including their use as an insecticide. Though there currently is no regulatory definition within the US as to what constitutes a nanoparticle insecticide, the term generally refers to anything that is 100 nm in size or smaller. The key feature that distinguishes a nanoinsecticide however, is that they demonstrate beneficial properties apart from the original material due to their small size. A number of studies have already demonstrated the toxic effects these metal nanoparticles possess against medically important mosquito vector species. However, the majority of studies have been limited to larvicidal efficacy and there has not yet been an in depth look into the use of metal nanoparticles as a potential adulticide. In this review, we summarize the current literature on the effectiveness of metal nanoparticles against adult mosquito vectors of medical importance. We also explore challenges for future research as well as potential pitfalls in evaluation methodology between existing studies.
Biosynthesis of metal nanoparticles as a mosquito control tool
Synthesizing a metal nanoparticle requires three separate components: a source of metal ions, a reducing agent and a capping or stabilizing agent (21). The combination of these three factors can greatly impact the physical characteristics, notably morphology and size, of the resulting nanoparticle (22). The objective of applying nanoparticle technology has been to enhance unique beneficial properties that many metals already demonstrate. For example, silver has been utilized as an antimicrobial treatment in medicine since the mid-twentieth century and low dose larval exposure to copper has been linked to longer larval development, lowered rates of eclosion and decreased larval fitness in mosquitoes (21, 23–26).
Increasingly, plants are being used in the production of metal nanoparticles due to their natural reducing and stabilizing potential. Plant-mediated synthesis, often referred to as green synthesis, is advantageous due to its simplicity as a single step reaction that does not require the use of intensive heat or chemical processing. Plant extracts are comprised of different phytochemicals, metabolites and volatile bioactive compounds, many of which have demonstrated toxic effects against mosquitoes acting as larvicides, pupicides, adulticides and repellents across a number of studies (27, 28). These compounds can disrupt receptor sites of the nervous system through different metabolic pathways. For example, alkaloids and monoterpenes act on Na+/K+ ion exchange while flavonoids target acetylcholinesterase (29). Additionally, plant extracts also demonstrate synergism with existing insecticides. Synergism screening has demonstrated enhanced adulticidal toxicity of permethrin when combined with Cyperus rotundus, Alpinia galanga and Cinnamomum verum essential oils (30). In 2013, Tong and Bloomquist identified six permethrin synergist essential oils whose mode of action was likely metabolic inhibition of enzymes cytochrome P450 monooxygenases and carboxylesterases (31). Plant-mediated metal nanoparticles, in theory, seek to incorporate the beneficial properties relevant for their use in insecticide application of both metal ions and plant extracts to improve control efficacy.
Metal nanoparticles are increasingly being explored for their use in mosquito control as a potential insecticide. Application of these particles against mosquitoes have proven to be quite effective across a wide range of studies (32, 33). An extensive review of more than 100 studies emphasizes the promising toxicity many biosynthesized metal nanoparticles demonstrate against the larvae and pupae of different mosquito species (32). Amongst these, selenium nanoparticles exhibited LC50 of 99.6, 104.13 and 240.7 µg/mL when administered to larvae of Anopheles stephensi (List.), Aedes aegypti (Linn.), and Culex quinquefasciatus (Say.) respectively while gold nanoparticles demonstrated slightly stronger toxicity with LC50 of 25.92 and 28.64 µg/mL against An. stephensi and Ae. aegypti respectively (34, 35). Similarly, silver nanoparticles (AgNP) synthesized via plant extracts have demonstrated a wide range of larvicidal efficacy against multiple species with LC50 values between 0.3 to 130.3 µg/mL (32, 33, 36–40).
Adulticidal efficacy of metal nanoparticles
While there have been many studies investigating the larvicidal efficacy of nanoparticles, few have investigated their effectiveness against adult mosquitoes. Table 1 summarizes findings of such studies conducted between 2011 and 2020. The majority of testing has focused on the adulticidal properties of AgNPs synthesized primarily via plant-mediated pathways against common mosquito vector species. Out of twenty-two identified studies, only two evaluated alternative metals (gold and zinc) and all but three used plant extracts as the reducing agents with the exception of fungal, bacterial and chemical synthesis pathways (Table 1). This disparity in metal choice is likely due to the low cost and availability of silver nitrate as alternative metal nanoparticles demonstrate comparable efficacy against adult mosquitoes. The gold nanoparticles evaluated against the malaria vector An. stephensi were demonstrated to have an LC50 at 11.23 µg/mL whereas zinc nanoparticles were shown to reduce longevity in the same mosquito species when exposed to concentration between 2-10 ppm (54, 61). All combinations of metal and reducing agent demonstrated toxic effects against mosquitoes. However, differences in material or reducing agent do not appear to produce noticeable differences in toxicity despite their role in determining physiochemical properties of the nanoparticle.
Table 1 Adulticidal toxicity of metal nanoparticles, their synthesis pathway and testing methodology against common mosquito vectors.
Feronia elephantum was used to synthesize AgNP which were evaluated against Ae. aegypti, An. stephensi and Cx. quinquefasciatus using the WHO susceptibility bioassay demonstrating LC50 values of 20.40, 18.04 and 21.80 µg/mL at 24h respectively (45). Similarly, nanoparticles synthesized from three other plant species, Chomelia asiatica, Zeuxine gracilis and Heliotropium indicum, were tested using the same methodology producing a range of LC50 between 8.48-32.23 µg/mL (46–48). The LC50 of Chenopodium ambrosioides synthesized AgNP tested against Ae. albopictus was determined to be 14.29 µg/mL (49). A series of studies conducted by Azarudeen et al. also confirmed comparable results using Hedyotis puberula, Ventilago maderaspatana and Naregamia alata to synthesize AgNPs (50–52). Of the studies conducted using the WHO tube bioassay, the lowest to highest LC50 achieved ranged from 6.68 to 48.94 µg/mL from AgNPs synthesized using Phyllanthus niruri and to V. maderaspatana respectively.
Although the majority of adulticide efficacy was evaluated using the WHO tube bioassay, several studies opted for alternative test methodologies. One study tested silver nanoparticles following WHO spatial spray guidelines against Cx. quinquefasciatus utilizing a fungal mediated synthesis yielding LC50 at 22h of 0.4 µl/cm2 (41). Bacteria mediated synthesis using Listeria monocytogenes, Bacillus subtilius and Streptomyces anulatus produced lower LC50 values at 0.16, 0.08 and 0.06 µl/cm2 respectively (43). Two additional studies evaluating AgNPs as a spatial spray also demonstrated comparable toxicity with an LC50 of Ficus religiosa synthesized particles at 0.12 µl/cm2 and Azadirachta indica at 0.53 µl/cm2 (42, 44). A modified CDC bottle bioassay study determined sodium citrate synthesized AgNPs induced 100% mortality at 4h post-treatment when applied to the bottles at 90 ppm (59). During the same study, nanoparticles conjugated with deltamethrin did not improve the treatment efficacy over a deltamethrin only control. Two separate studies conducted against Ae. aegypti and An. stephensi also confirmed sub-lethal exposure to AgNPs reduced adult longevity in both male and female mosquitoes.
Future challenges: standardizing evaluation methodology and broadening research scope
Preliminary studies on metal nanoparticle adulticides have shown promising results which warrant further research and discussion on how to potentially integrate this technology as a mosquito control tool. This is necessary because adulticides are the primary tool used to curb active transmission of mosquito-borne disease, yet there are so few available insecticidal AIs when compared to larviciding. Increasing levels of insecticide resistance across mosquito populations globally have also diminished the potency of current insecticides and new AIs are needed to maintain effectiveness of mosquito control operations. However, our review of the current literature on metal nanoparticle adulticides exposes several key issues that should be addressed in future testing. These include inconsistent testing methodology, an unknown mode of action, absence of field efficacy trials and unexplored interactions with existing insecticides.
First, there is no consistency in methodology for evaluating the toxicity of nanoparticles. According to WHO guidelines, the effectiveness of a novel insecticide must be assessed across three phases of testing: (1) inherent toxicity evaluations, (2) small-scale studies and outdoor semi-field applications and (3) operational trials against field populations with before and after measurements of mosquito population abundance (63). Due to their novelty in mosquito control research, metal nanoparticles have so far been limited to the first phase of testing.
For laboratory trials, the standard measure of intrinsic toxicity is through the direct topical application of a given insecticide to the pronotum across a range of concentrations to determine the lethal dose. This is typically supplemented with additional testing to determine its insecticidal activity as a spatial spray. Here, an insecticide is atomized to produce droplets of a known size into a wind tunnel and again, administered to test mosquitoes across a range of concentrations to calculate lethal concentration.
In the current literature however, a majority of researchers have opted to use the WHO tube bioassay and the CDC bottle bioassay as alternative methodologies. Briefly, the WHO tube bioassay employs a tarsal contact test scheme. In this evaluation, filter paper is impregnated with a known concentration of an insecticide and placed into a tube. Mosquitoes are then introduced into the tube where they are exposed to the impregnated filter paper for one hour, after which they are transferred into a separate clean holding tube where they can be observed for mortality. Similarly, the CDC bottle bioassay also employs the same tarsal contact scheme using glass bottles whose interior surface are treated with a known concentration of insecticide dissolved into a solvent such as acetone. After the bottles have dried, mosquitoes can be introduced and assessed for mortality.
More than half of the twenty-two studies reviewed in this article were conducted using the WHO tube bioassay. Of the remaining studies, four tested the metal nanoparticles as a spatial spray, one using the CDC bottle bioassay and one using fabrics impregnated with silver nanoparticles. In the latter study, mosquitoes were exposed to the impregnated fabrics using the same contact and holding methodology as the WHO tube bioassay. This diverse assortment of studies is problematic because the results cannot be directly compared. Furthermore, the WHO tube bioassay and CDC bottle bioassay are not representative of how mosquitoes would interact with the nanoparticles in real world applications. Adulticide treatments are primarily delivered as a spatial spray where individual droplets must come into physical contact with a mosquito. Prolonged tarsal contact schemes are more suited for testing residual insecticides but are not an appropriate proxy for adulticide sprays. Data generated in these studies would therefore not comply with registration requirements for novel insecticides. For these reasons, lethal dose and lethal concentration as determined by direct topical applications and spatial spray testing following WHO guidelines would provide optimal metrics by which to judge the efficacy of any new insecticide. As further research into metal nanoparticle insecticides progress, testing needs to be standardized to ensure any obtained data can be compared between studies.
Second, although metallic nanoparticles have demonstrated strong efficacy to control mosquitoes at all life stages, their mode of action has yet to be definitively determined. One hypothesis is that metal nanoparticles act on cellular membranes and detoxification enzymes which leads to loss of cellular function and eventual death (32, 64). However, the mechanism by which nanoparticles induce mortality has yet to be fully explored and further research is needed. Third, testing should be expanded to include field collected populations and insecticide resistant colonies to better validate the potential operational efficacy of metal nanoparticle adulticides amidst the rising prevalence of insecticide resistance. Fourth, the scope of research should be broadened not only to stand-alone effects but also how the metal nanoparticles interact with existing insecticides. This could conceivably include their role as an additive insecticidal agents but also as nanocarrier delivery systems for conventional insecticides (65). In one such study, deltamethrin was successfully conjugated with silver nanoparticles (59). Although this did not improve treatment efficacy above the deltamethrin control, investigating potential synergism presents a promising avenue of research.
In summary, preliminary studies on metal nanoparticle adulticides have shown promising results but are hindered by inconsistent testing methodology, preventing meaningful comparisons between studies. Additionally, the mode of action, field study results and synergism with existing insecticides remains largely unexplored. Future research efforts should seek to address these areas. Plants possess bioactive compounds including alkaloids, ketones, tannins and essential oils which have demonstrated insecticidal effects, but many of these same compounds can also act as synergists with existing insecticides (66, 67). By synthesizing metal nanoparticles in conjunction with these bioactive compounds, researchers aim to confer beneficial properties to enhance insecticide formulations, thus providing potential new tool in managing resistance in mosquito populations.
Author contributions
KB was responsible for conceptualizing the topic being review and for drafting the manuscript. All authors contributed to revision of the manuscript and have approved the submitted version.
Funding
Publication fees were provided by grant funding through Florida Department of Agriculture and Consumer Services, AWD11192: Evaluation of a nanoparticle encapsulated permethrin formulation against three species of adult mosquitoes: Aedes aegypti, Culex quinquefasciatus and Anopheles quadrimaculatus.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
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Keywords: silver nanoparticle, metal nanoparticle, adulticide, AgNP, green synthesis, nanoinsecticide, nanotechnology
Citation: Blore K, Baldwin R, Batich CD, Koehler P, Pereira R, Jack CJ, Qualls WA and Xue RD (2022) Efficacy of metal nanoparticles as a control tool against adult mosquito vectors: A review. Front. Trop. Dis 3:969299. doi: 10.3389/fitd.2022.969299
Received: 14 June 2022; Accepted: 08 August 2022;
Published: 31 August 2022.
Edited by:
Indra Vythilingam, University of Malaya, MalaysiaReviewed by:
Luc Salako Djogbénou, Université d’Abomey-Calavi, BeninRajnikant Dixit, National Institute of Malaria Research (ICMR), India
Copyright © 2022 Blore, Baldwin, Batich, Koehler, Pereira, Jack, Qualls and Xue. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Kai Blore, kblore@amcdfl.org