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Preplanned Studies: Laboratory and Semi-Field Evaluation on S-Methoprene Formulations Against Anopheles sinensis (Diptera: Culicidae) — Yuxi City, Yunnan Province, China

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  • Summary

    What is already known about this topic?

    Anopheles sinensis (An. sinensis) is the predominant malaria vector in China. The impact of S-methoprene on the emergence process of mosquito larvae suggests its potential as a control method for vector mosquitoes. However, the efficacy of S-methoprene in controlling An. sinensis has not yet been demonstrated.

    What is added by this report?

    The effectiveness of S-methoprene against An. sinensis was assessed in laboratory and semi-field conditions in Yunnan Province.

    What are the implications for public health practice?

    These results offer valuable options and guidance for utilizing S-methoprene products in malaria reimportation prevention areas within Yunnan Province.

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  • Funding: Project on the Establishment of China-ASEAN Science and Technology Cooperation Center for Public Health (KY202101004) funded by The National Key Research and Development Program of China
  • [1] World Health Organization. World malaria report 2022. Geneva: World Health Organization; 2022. https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2022.
    [2] Feng XY, Zhang SS, Huang F, Zhang L, Feng J, Xia ZG, et al. Biology, bionomics and molecular biology of Anopheles sinensis Wiedemann 1828 (Diptera: Culicidae), main malaria vector in China. Front Microbiol 2017;8:1473. https://doi.org/10.3389/fmicb.2017.01473.
    [3] Barua A, Williams CD, Ross JL. A literature review of biological and bio-rational control strategies for slugs: current research and future prospects. Insects 2021;12(6):541. https://doi.org/10.3390/insects12060541.
    [4] Cui LW, Yan GY, Sattabongkot J, Cao YM, Chen B, Chen XG, et al. Malaria in the greater Mekong Subregion: heterogeneity and complexity. Acta Trop 2012;121(3):227 − 39. https://doi.org/10.1016/j.actatropica.2011.02.016.
    [5] Henrick CA. Methoprene. J Am Mosq Control Assoc 2007;23(S2):225 − 39. https://doi.org/10.2987/8756-971X(2007)23[225:M]2.0.CO;2.
    [6] Su TY. Research, development and application of s-methoprene in the USA – 50 years of excellence. Chin J Hyg Insectic Equip 2018;24(4):317 − 25. https://doi.org/10.19821/j.1671-2781.2018.04.001.
    [7] Zhou YW, Luo ZS, Lin ZR, Xu JW, Xu SY, Shi J, et al. Anopheles sinensis mutations and resistance to common insecticides in Cangyuan County, Yunnan Province, China Myanmar border area. Chin J Zoonoses 2023;39(3):289 − 93,298. https://doi.org/10.3969/j.issn.1002-2694.2023.00.011.
    [8] Su TY, Thieme JL, Cheng ML. Impact of storage and handling temperatures on the activities of mosquito larvicides. J Am Mosq Control Assoc 2018;34(3):244 − 8. https://doi.org/10.2987/18-6770.1.
    [9] Hua NZ. Development and rencent progess of pesticide miroencapusulates. Modern Agrochemicals 2010,9(03):10-14,18.
    [10] Tsai WT, Lai CW, Hsien KJ. Characterization and adsorption properties of diatomaceous earth modified by hydrofluoric acid etching. J Colloid Interface Sci 2006;297(2):749 − 54. https://doi.org/10.1016/j.jcis.2005.10.058.
  • FIGURE 1.  Semi-field testing site in Yuxi City, Yunnan Province. (A) Microcosms; (B) Assembled sentinel cage.

    FIGURE 2.  Inhibition of emergence (IE) against Anopheles sinensis by S-methoprene products with a water depth of 13.0 cm.

    TABLE 1.  Laboratory bioassays on S-methoprene technical material and products against Anopheles sinensis.

    Product IE 10 (μg/L) (95% CI) IE50 (μg/L) (95% CI) IE 90 (μg/L) (95% CI)
    Technical S-methoprene 0.055 (0.012–1.060) 0.220 (0.119–0.303) 0.883 (0.640–1.529)
    microencapsulated suspension 0.046 (0.019–0.076) 0.236 (0.017–0.322) 1.199 (0.744–2.893)
    1% granule 0.052 (0.009–1.065) 0.221 (0.116–0.331) 1.238 (0.885–3.840)
    Note: Mortality data was corrected by factoring the mortality in untreated control (6.4%–8%) using Abbott formula (Abbott, 1925) before probit analysis.
    Abbreviation: CI=confidence intervals; IE=inhibition of emergence.
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Laboratory and Semi-Field Evaluation on S-Methoprene Formulations Against Anopheles sinensis (Diptera: Culicidae) — Yuxi City, Yunnan Province, China

View author affiliations

Summary

What is already known about this topic?

Anopheles sinensis (An. sinensis) is the predominant malaria vector in China. The impact of S-methoprene on the emergence process of mosquito larvae suggests its potential as a control method for vector mosquitoes. However, the efficacy of S-methoprene in controlling An. sinensis has not yet been demonstrated.

What is added by this report?

The effectiveness of S-methoprene against An. sinensis was assessed in laboratory and semi-field conditions in Yunnan Province.

What are the implications for public health practice?

These results offer valuable options and guidance for utilizing S-methoprene products in malaria reimportation prevention areas within Yunnan Province.

  • 1. School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan City, Shandong Province, China
  • 2. National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, WHO Collaborating Centre for Vector Surveillance and Management, Department of Vector Biology and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
  • 3. EcoZone International, Riverside City, CA, USA
  • 4. Department of Environment and Health, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan City, Shandong Province, China
  • 5. Department of Vector Control, School of Public Health, Shandong University, Ji’nan City, Shandong Province, China
  • 6. Xinjiang Key Laboratory of Vector-borne Infectious Diseases, Urumqi City, Xinjiang, 830002
  • Corresponding authors:

    Xiaobo Liu, liuxiaobo@icdc.cn

    Tianyun Su, stevensu1995@gmail.com

    Qiyong Liu, liuqiyong@icdc.cn

  • Funding: Project on the Establishment of China-ASEAN Science and Technology Cooperation Center for Public Health (KY202101004) funded by The National Key Research and Development Program of China
  • Online Date: February 09 2024
    Issue Date: February 09 2024
    doi: 10.46234/ccdcw2024.023
  • Malaria is an infectious disease transmitted by mosquitoes, specifically through the bite of Anopheles mosquitoes or by blood transfusion from an infected person. In 2021, there were approximately 247 million malaria cases reported in 84 countries endemic to malaria (1).

    The most common mosquito species responsible for malaria transmission in China is Anopheles sinensis (An. sinensis) Wiedemann (2). Chemical control is currently a primary method for comprehensive vector management due to its simplicity, effectiveness, and ease of use. However, the emergence of pesticide resistance among malaria vector mosquitoes has become a significant concern. Yunnan Province, located in the Greater Mekong subregion (GMS), is particularly vulnerable as a malaria hotspot (3). Studies have demonstrated that An. sinensis mosquitoes in Yuxi City, Yunnan Province have developed resistance to traditional chemical insecticides like organophosphorus, carbamate, organochlorines, and pyrethroids (4).

    In recent years, biological control has gained attention in the field of entomology and vector control as a potential solution to pesticide resistance. One notable biological insecticide is the juvenile hormone analogue S-methoprene, which has been used in the United States since the 1970s and is recognized for its efficacy against various vector species while maintaining environmental safety and non-target organism protection (5). Several formulations of S-methoprene, including emulsifiable concentrate, microcapsule suspensions, granules, pellets, water-soluble pouches, and briquets (6).

    S-methoprene technical material and its products were tested in a laboratory against late-instar larvae of An. sinensis. Following this, an experimental site in Yuxi City, Yunnan Province (Figure 1) was selected to evaluate the impacts of different formulations of S-methoprene products on An. sinensis under semi-field conditions (Supplementary Material). The bioassays showed that the formulated products and technical material had similar efficacy in inhibiting adult emergence at three different IE levels. Under semi-field conditions, a 20% microcapsule suspension at a dosage of 0.025–0.1 mL/m2 provided 100% efficacy for at least 3 days, while 1% granules at9.09 g/m2 and 4.3% granules at 2.0 g/m2 providedmore than 85% efficacy for at least 14 days. The results confirmed the strong biological activity and safety profile of S-methoprene, supporting its recommendation as a standard larvicidal tool for controlling An. sinensis in various habitats while adhering to local regulations.

    Figure 1. 

    Semi-field testing site in Yuxi City, Yunnan Province. (A) Microcosms; (B) Assembled sentinel cage.

    In the concurrent bioassays, we tested the effectiveness of S-methoprene technical material, microencapsulated suspension, and two granules against An. sinensis. The results showed that all formulations exhibited high activity in inhibiting adult emergence. Interestingly, there were no significant differences observed between the formulated products and the pure S-methoprene technical material at three different application levels. This data is summarized in Table 1.

    Product IE 10 (μg/L) (95% CI) IE50 (μg/L) (95% CI) IE 90 (μg/L) (95% CI)
    Technical S-methoprene 0.055 (0.012–1.060) 0.220 (0.119–0.303) 0.883 (0.640–1.529)
    microencapsulated suspension 0.046 (0.019–0.076) 0.236 (0.017–0.322) 1.199 (0.744–2.893)
    1% granule 0.052 (0.009–1.065) 0.221 (0.116–0.331) 1.238 (0.885–3.840)
    Note: Mortality data was corrected by factoring the mortality in untreated control (6.4%–8%) using Abbott formula (Abbott, 1925) before probit analysis.
    Abbreviation: CI=confidence intervals; IE=inhibition of emergence.

    Table 1.  Laboratory bioassays on S-methoprene technical material and products against Anopheles sinensis.

    During the testing period, the infection rate (IE) of An. sinensis against IE in untreated control (UTC) was as low as 0–4%. The experimental endpoint was considered achieved when the IE provided by the insecticidal preparations was less than 85%. There were dose-dependent and time-related effectiveness trends observed within the intended range of 0.025–0.1 mL/m2. On the third day of the evaluation period, all three selected concentrations showed 100% efficacy. However, on the 7th day of assessment, the IE decreased to 48% at 0.025 mL/m2 and 52% at 0.038 mL/m2. For the highest concentration of 0.1 mL/m2, assessments were conducted from day 14 until the experimental endpoint (Figure 2). The IE% showed a highly significant difference among the UTC and treatment groups (χ2=193.2–250.0, P<0.001), as well as among the doses on days 3, 7/14 (χ2=10.4–18.9, P<0.01).

    Figure 2. 

    Inhibition of emergence (IE) against Anopheles sinensis by S-methoprene products with a water depth of 13.0 cm.

    Dose-dependent and time-related effectiveness trends were observed within the intended range of 1.60–9.09 g/m2. On the third day of the evaluation period, all three selected concentrations demonstrated 100% efficacy. However, at a concentration of 1.60 g/m2, the effectiveness persisted for less than 7 days. By the 14th day of assessment, the effectiveness decreased to 38% at 5.13 g/m2 and 86% at 9.09 g/m2. For the highest concentration of 9.09 g/m2, assessments were continued from day 21 until the end of the experiment (Figure 2). The effectiveness percentage (IE%) showed significant differences among the UTC and treatment groups (χ2=150.9–250.0, P<0.001), as well as among the different doses on days 3, 14–21 (χ2= 9.33–11.27, P<0.01).

    Dose-dependent and time-related trends in effectiveness were observed within the intended range of 0.4–2 g/m2. By the third day of evaluation, all three selected concentrations showed 100% efficacy. At a concentration of 0.4 g/m2, the duration of effectiveness was less than 7 days. On the 7th day of evaluation, all concentrations showed 100% efficacy. On the 21st day, the effectiveness decreased to 76% at 1.0 g/m2 and 80% at 2.0 g/m2. The effectiveness percentages were significantly different among the untreated control group and the various treatments (χ2=145.7–250.0, P<0.001) and among the doses on days 3, 14–21 (χ2=27.78–31.86, P<0.01).

    • The Greater Mekong Subregion (GMS), which includes Yunnan Province of China, Cambodia, Lao PDR, Myanmar, Thailand, and Vietnam, is a significant malaria hotspot. The introduction of the Mekong Malaria Program (MRP) by the World Health Organization (WHO) has led to notable improvements in malaria control in the region, with a consistent decrease in annual malaria incidence and deaths (4).

      Integrated mosquito control, combining environmental management and targeted pesticide use, is essential for reducing mosquito populations and controlling mosquito-borne diseases. Larviciding, which targets the aquatic stages of mosquitoes, is a cost-effective approach in mosquito control compared to adulticiding, which targets adult mosquitoes.

      For example, in a study by Zhou et al., it was found that An. sinensis, the malaria vector, has developed high resistance to conventional chemical insecticides such as beta-cypermethrin and propoxur in Yunnan Province (7).

      Over the past 50 years, the USA has established the advantages of S-methoprene against economically significant pests in public health, livestock, stored goods, and agriculture (6). However, S-methoprene is rarely used in China, with only the Synergetica Life Science Changzhou company producing S-methoprene products. It rapidly degrades in soil, particularly under sunlight, with a half-life of 10–14 days. The primary microbial degradation product is carbon dioxide (8).

      To cater to various application scenarios, S-methoprenate products have been developed in multiple forms, with granules and microencapsulated suspensions being the most popular. The milky white turbid microcapsule suspension, diluted with water, was utilized with spraying equipment. The granules used granulated as a natural carrier with a diameter of 1.0–2.0, which was doubled using a specialized binding technique. Both products were extensively evaluated against the index species, utilizing late fourth instar larvae in laboratory and field studies. These larvae, prior to pupation, exhibit high susceptibility to external JHAs due to low levels of internally present juvenile hormone III. The comparable efficacy of the formulations with the S-methoprene technical materials in bioassays justified further field evaluation for both the granules and microencapsulated suspensions.

      The formulated S-methoprene product showed the desired initial and residual efficacy against An. sinensis. Microcapsules were used at concentrations of 0.025 mL/m2, 0.038 mL/m2, and 0.1 mL/m2, effectively controlling An. sinensis for a minimum of 3 days at a water depth of 13 cm. Granules, on the other hand, exhibited longer persistence. The 1% granules provided over 85% control for at least 14 days at a concentration of 9.09 g/m2. Similarly, at doses of 1.0 g/m2 and 2.0 g/m2, the 4.3% granules maintained at least 85% control for 14 days. It is worth noting that microencapsulated suspension and granules have distinct characteristics and are suited for different scenarios. The effectiveness observed can be attributed to the special carrier system, which ensures proper binding, preservation, and transport of the active ingredient. In the case of microcapsule suspension, the methoprene ester is coated within the capsule shell, providing protection against light damage and extending the effectiveness period (9). The granules, composed of fossilized diatoms, possess a high water absorption capacity and a large surface area, reducing exposure of the active ingredient to ultraviolet radiation and microbial activity in aquatic ecosystems (10).

      This study has several limitations primarily due to the semi-field evaluation approach. First, the study excluded factors such as rainfall and sunlight exposure and instead created more controlled microcosms. Additionally, the capture of An. sinensis larvae in the field may introduce inevitable systematic errors, as less motile larvae are more likely to be captured.

      There is an urgent need to find alternatives to conventional chemical pesticides to address the problem of mosquito resistance, specifically with larvicides that are effective and cost-efficient. S-methoprene has been shown to be safe for non-target organisms and environmentally friendly. Considering its proven performance against An. sinensis and its ability to adapt to different scenarios, it would be reasonable to recommend S-methoprene as a standard larvicidal tool for various mosquito habitats, while complying with local regulations.

    • No conflicts of interest.

    • All local farmer families who participated in this study and the staff of Yuanjiang County Center for Disease Control and Prevention and Ganzhuang Subdistrict Health Center.

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