Can insecticide resistance status affect parasite transmission in mosquitoes?

https://doi.org/10.1016/S0965-1748(02)00097-8Get rights and content

Introduction

The primary means of controlling mosquito-borne diseases such as malaria and filariasis is still by residual spraying with insecticides. The development of insecticide resistance in mosquito vectors is common (Hemingway and Ranson, 2000). Culex quinquefasciatus uses one predominant esterase-based organophosphate resistance mechanism that occurs in more than 80% of insecticide-resistant Culex worldwide (Hemingway and Karunaratne, 1998, Raymond et al., 1991). The commonest variant of this mechanism originated once before spreading rapidly to all continents (Raymond et al., 1991). This resistance depends on the stable germline amplification of two esterase enzymes and an aldehyde oxidase encoded on a 30 kilobase DNA amplicon (Hemingway et al., 2000). Up to 80 copies of this amplicon can be present per cell in resistant mosquitoes (Paton et al., 2000). In Anopheles mosquitoes there is a wider variety of insecticide resistance mechanisms, with elevated glutathione S-transferases producing DDT resistance (Ranson et al., 2000, Prapanthadara et al., 1995), and elevated P450 monooxygenases combined with an altered sodium channel (kdr) contributing to pyrethroid resistance (Chandre et al., 2000, Vulule et al., 1999) and elevated esterases and altered malathion carboxylesterases producing general organophosphorus and malathion specific resistance respectively (Brogdon and Barber, 1990, Hemingway, 1982).

Insecticide resistance is assumed to increase the likelihood of mosquito-borne disease transmission by increasing the vector population size and allowing mosquitoes to live longer in the presence of insecticide. The validity of this assumption was recently tested using Sri Lankan C. quinquefasciatus and lymphatic filariasis as a model system (McCarroll et al., 2000).

Vectorial capacity i.e. the ability of mosquitoes to ingest parasites and to promote their maturation until the infective stage, and the rate of mosquito survival until parasite maturation (Failloux et al., 1995), can differ according to geographic mosquito strain (Crans, 1973, McGreevy et al., 1982). No attempt has previously been made to explain these geographical differences, but one influence may be insecticide selection pressure. It is assumed that insecticide resistance increases the size and mean longevity of the vector population in the presence of insecticide, thus increasing disease transmission. However, many questions remain unresolved on the evolutionary fitness costs and vectorial capacity of insects which are resistant to insecticides (Ferdig et al., 1993, Kraaijeveld and Godfrey, 1997, Yan et al., 1997). In insecticide resistant C. quinquefasciatus, esterases are highly expressed in the midgut, subcuticular layer, Malpighian tubules and salivary glands, resulting in a change in the redox potential in these cells compared to their susceptible counterparts (Hemingway, 2000). As most mosquito-borne parasites must pass through some of these tissues to complete their development, it is possible that parasite survival, and hence the vectorial capacity of the insect, may be directly affected by the insecticide status of the insects. The study by McCarroll et al. (2000) was the first to attempt to examine directly the relationship between vectorial capacity and insecticide resistance within an insect population.

Section snippets

Filariasis infection rates in Sri Lankan Culex

Sri Lanka is endemic for periodic lymphatic filariasis caused by the parasitic worm Wuchereria bancrofti. Random surveys of Sri Lankan C. quinquefasciatus previously demonstrated a low incidence (0.6%) of L3 filarial larvae in the mosquito field population (Hawking, 1976). To obtain a large naturally infected field-collected sample, we would have needed to analyse very large numbers of randomly collected insects, which was not feasible. To ensure that the majority of mosquitoes collected were

Are insecticide resistance and parasite infection rates independent?

A quantitative PCR (QPCR) approach, based on the detection system described above, was developed in our study to detect W. bancrofti-infected insects. QPCR using a Lightcycler (Roche) enabled rapid detection and quantification of specific filarial worm DNA sequence. Incorporation of the double-strand-specific fluorescent dye, SYBR Green I, allowed the detection of PCR product formation and accumulation. The fluorescence incorporated into the PCR product was measured at the end of the extension

Is this negative correlation in L1 filarial larval infections and insecticide resistance reflected in the numbers of infective larvae developing in resistant insects?

In parallel with the fieldwork, laboratory colonies of four-day-old adult female insecticide-resistant (PelRR) and susceptible (PelSS) Sri Lankan C. quinquefasciatus mosquitoes were fed with W. bancrofti-infected blood which had an intermediate level of parasitaemia. These colonies were derived from a field population, heterogeneous for resistance in 1997. The populations were selected for high and low esterase activity as described previously by Peiris and Hemingway (1993) for earlier

Does insecticide resistance actually affect filariasis disease transmission in Sri Lanka?

It is unclear from our present data whether insecticide-resistant C. quinquefasciatus mosquitoes in the field are less likely to transmit filariasis than their insecticide-susceptible counterparts since the development of a single mature filaria is sufficient to cause disease transmission. Our laboratory study suggests that L3 infective larvae are unable to develop in highly resistant C. quinquefasciatus. However, it should be noted that this laboratory colony, although derived from the same

Acknowledgements

We thank Dr. Philippe Esterre, Head of Immunology Unit, Institut de Recherches Médicales L. Malardé BP30 99713—Papeete, Tahiti/French Polynesia for supplying W. bancrofti plasmids and DNA.

First page preview

First page preview
Click to open first page preview

References (38)

  • W.J. Crans

    Experimental infection of Anopheles gambiae and Culex pipiens fatigans with Wuchereria bancrofti in coastal East Africa

    J Med Entomol.

    (1973)
  • Dassanayake, V.D., 1998. Insecticide resistance of Culex quinquefasciatus Say (Dipter Culicidae) in Sri Lanka. MPhil...
  • A.B. Failloux et al.

    Variation in the vector competence of Aedes polynesiensis for Wuchereria bancrofti

    Parasitology

    (1995)
  • M.T. Ferdig et al.

    Reproductive costs associated with resistance in a mosquito-filarial worm system

    Am J Trop Med Hyg

    (1993)
  • F. Hawking

    The distribution of human filariasis throughout the world, Part II

    Asia. Trop Dis Bull

    (1976)
  • J. Hemingway

    Genetics of organophosphate and carbamate resistance in Anopheles atroparvus (Diptera:Culicidae)

    J Econ Entomol.

    (1982)
  • J. Hemingway et al.

    Mosquito carboxylesterases: A review of the molecular biology and biochemistry of a major insecticide resistance mechanism

    Med Vet Entomol

    (1998)
  • J. Hemingway et al.

    Insecticide resistance in insect vectors of human disease

    Ann Rev Entomol

    (2000)
  • J. Hemingway et al.

    Aldehyde oxidase is coamplified with the world’s most common Culex mosquito insecticide resistance-associated esterases

    Ins Mol Biol

    (2000)
  • Cited by (68)

    • First comprehensive report of the resistance of Culex quinquefasciatus Say (Diptera: Culicidae) to commonly used insecticides in Riyadh, Saudi Arabia

      2023, Heliyon
      Citation Excerpt :

      quinquefasciatus [12], chemical approaches are the main strategies for controlling this insect vector to prevent transmission of the associated diseases [13,14]. For decades, organophosphates (OPs) and pyrethroids have been the most commonly used insecticides globally to control mosquitoes, and they can be administered using different modalities including indoor residual sprays, space spraying, and mosquito coils [12]. In Riyadh province, Saudi Arabia, mosquito control programs are conducted on a seasonal basis (spring: March to May, fall: September to November) because of its severe desert climate, and in most cases, insecticides are applied once monthly [15].

    • Malathion-resistant Tribolium castaneum has enhanced response to oxidative stress, immunity, and fitness

      2022, Pesticide Biochemistry and Physiology
      Citation Excerpt :

      Organophosphate resistant individuals of the mosquito, C. pipiens, had a greater load of bacteria Wolbachia than the susceptibles, showing a greater fitness cost (Berticat et al., 2002). In another mosquito (C. quinquefasciatus) with a high level of an esterase resistance mechanism the transmission of filariasis was strongly reduced (McCarroll and Hemingway, 2002). Research on C. pipiens and the obligate parasite Vavraia culicis, that kills its host before adult eclosion, compared organophosphate resistant and susceptible strains (Agnew et al., 2004).

    • Effects of insecticide resistance and exposure on Plasmodium development in Anopheles mosquitoes

      2020, Current Opinion in Insect Science
      Citation Excerpt :

      Furthermore chemical synergists such as piperonyl butoxide (PBO) [42], which inhibits the activity of detoxification enzymes and that can be added to pyrethroid-treated surfaces to combat metabolic resistance, may affect how these mechanisms impact on Plasmodium. Changes in the midgut redox conditions may explain the reported detrimental effects of metabolic resistance or exposure to xenobiotics and insecticides on the midgut stages of filarial [7] and malaria [28,32••,33] parasites. Since ROS/RNS also act as both effectors and mediators in Anopheles anti-plasmodial immunity systemically and specifically in the midgut lumen and epithelium [35], changes in their amount may have pleiotropic effects on other immune responses.

    View all citing articles on Scopus
    View full text