Insecticide resistance status of  Aedes aegypti  and  Aedes albopictus  mosquitoes in Papua New Guinea

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Abstract

Background

Aedes aegypti and Ae. albopictus are important vectors of infectious diseases, especially those caused by arboviruses such as dengue, chikungunya and Zika. Aedes aegypti is very well adapted to urban environments, whereas Ae. albopictus inhabits more rural settings. Pyrethroid resistance is widespread in these vectors, but limited data exist from the Southwest Pacific Region, especially from Melanesia. While Aedes vector ecology is well documented in Australia, where incursion of Ae. albopictus and pyrethroid resistance have so far been prevented, almost nothing is known about Aedes populations in neighbouring Papua New Guinea (PNG). With pyrethroid resistance documented in parts of Indonesia but not in Australia, it is important to determine the distribution of susceptible and resistant Aedes populations in this region.

Methods

The present study was aimed at assessing Aedes populations for insecticide resistance in Madang and Port Moresby, located on the north and south coasts of PNG, respectively. Mosquitoes were collected using ovitraps and reared in an insectary. Standard WHO bioassays using insecticide-treated filter papers were conducted on a total of 253 Ae. aegypti and 768 Ae. albopictus adult mosquitoes. Subsets of samples from both species (55 Ae. aegypti and 48 Ae. albopictus) were screened for knockdown resistance mutations in the voltage-sensitive sodium channel ( Vssc) gene, the target site of pyrethroid insecticides.

Results

High levels of resistance against pyrethroids were identified in Ae. aegypti from Madang and Port Moresby. Aedes albopictus exhibited susceptibility to pyrethroids, but moderate levels of resistance to DDT. Mutations associated with pyrethroid resistance were detected in all Ae. aegypti samples screened. Some genotypes found in the present study had been observed previously in Indonesia. No Vssc mutations associated with pyrethroid resistance were found in the Ae. albopictus samples.

Conclusions

To our knowledge, this is the first report of pyrethroid resistance in Ae. aegypti mosquitoes in PNG. Interestingly, usage of insecticides in PNG is low, apart from long-lasting insecticidal nets distributed for malaria control. Further investigations on how these resistant Ae. aegypti mosquito populations arose in PNG and how they are being sustained are warranted.

Electronic supplementary material

The online version of this article (10.1186/s13071-019-3585-6) contains supplementary material, which is available to authorized users.

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Most cited references 29

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Pyrethroid resistance in Aedes aegypti and Aedes albopictus: Important mosquito vectors of human diseases.

Leticia Smith, Shinji Kasai, Jeffrey G Scott (2016)

Aedes aegypti and A. albopictus mosquitoes are vectors of important human disease viruses, including dengue, yellow fever, chikungunya and Zika. Pyrethroid insecticides are widely used to control adult Aedes mosquitoes, especially during disease outbreaks. Herein, we review the status of pyrethroid resistance in A. aegypti and A. albopictus, mechanisms of resistance, fitness costs associated with resistance alleles and provide suggestions for future research. The widespread use of pyrethroids has given rise to many populations with varying levels of resistance worldwide, albeit with substantial geographical variation. In adult A. aegypti and A. albopictus, resistance levels are generally lower in Asia, Africa and the USA, and higher in Latin America, although there are exceptions. Susceptible populations still exist in several areas of the world, particularly in Asia and South America. Resistance to pyrethroids in larvae is also geographically widespread. The two major mechanisms of pyrethroid resistance are increased detoxification due to P450-monooxygenases, and mutations in the voltage sensitive sodium channel (Vssc) gene. Several P450s have been putatively associated with insecticide resistance, but the specific P450s involved are not fully elucidated. Pyrethroid resistance can be due to single mutations or combinations of mutations in Vssc. The presence of multiple Vssc mutations can lead to extremely high levels of resistance. Suggestions for future research needs are presented.

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Molecular evidence for dual pyrethroid-receptor sites on a mosquito sodium channel.

Boris Zhorov, Crystal Y. Q. Du, Gul Satar … (2013)

Pyrethroid insecticides are widely used as one of the most effective control measures in the global fight against agricultural arthropod pests and mosquito-borne diseases, including malaria and dengue. They exert toxic effects by altering the function of voltage-gated sodium channels, which are essential for proper electrical signaling in the nervous system. A major threat to the sustained use of pyrethroids for vector control is the emergence of mosquito resistance to pyrethroids worldwide. Here, we report the successful expression of a sodium channel, AaNav1-1, from Aedes aegypti in Xenopus oocytes, and the functional examination of nine sodium channel mutations that are associated with pyrethroid resistance in various Ae. aegypti and Anopheles gambiae populations around the world. Our analysis shows that five of the nine mutations reduce AaNav1-1 sensitivity to pyrethroids. Computer modeling and further mutational analysis revealed a surprising finding: Although two of the five confirmed mutations map to a previously proposed pyrethroid-receptor site in the house fly sodium channel, the other three mutations are mapped to a second receptor site. Discovery of this second putative receptor site provides a dual-receptor paradigm that could explain much of the molecular mechanisms of pyrethroid action and resistance as well as the high selectivity of pyrethroids on insect vs. mammalian sodium channels. Results from this study could impact future prediction and monitoring of pyrethroid resistance in mosquitoes and other arthropod pests and disease vectors.

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Insecticide Resistance Status of United States Populations of Aedes albopictus and Mechanisms Involved

Sébastien Marcombe, Ary Farajollahi, Sean P. Healy … (2014)

Aedes albopictus (Skuse) is an invasive mosquito that has become an important vector of chikungunya and dengue viruses. Immature Ae. albopictus thrive in backyard household containers that require treatment with larvicides and when adult populations reach pest levels or disease transmission is ongoing, adulticiding is often required. To assess the feasibility of control of USA populations, we tested the susceptibility of Ae. albopictus to chemicals representing the main insecticide classes with different modes of action: organochlorines, organophosphates, carbamates, pyrethroids, insect growth regulators (IGR), naturalytes, and biolarvicides. We characterized a susceptible reference strain of Ae. albopictus, ATM95, and tested the susceptibility of eight USA populations to five adulticides and six larvicides. We found that USA populations are broadly susceptible to currently available larvicides and adulticides. Unexpectedly, however, we found significant resistance to dichlorodiphenyltrichloroethane (DDT) in two Florida populations and in a New Jersey population. We also found resistance to malathion, an organophosphate, in Florida and New Jersey and reduced susceptibility to the IGRs pyriproxyfen and methoprene. All populations tested were fully susceptible to pyrethroids. Biochemical assays revealed a significant up-regulation of GSTs in DDT-resistant populations in both larval and adult stages. Also, β-esterases were up-regulated in the populations with suspected resistance to malathion. Of note, we identified a previously unknown amino acid polymorphism (Phe → Leu) in domain III of the VGSC, in a location known to be associated with pyrethroid resistance in another container-inhabiting mosquito, Aedes aegypti L. The observed DDT resistance in populations from Florida may indicate multiple introductions of this species into the USA, possibly from tropical populations. In addition, the mechanisms underlying DDT resistance often result in pyrethroid resistance, which would undermine a remaining tool for the control of Ae. albopictus. Continued monitoring of the insecticide resistance status of this species is imperative.

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Author and article information

Contributors

Samuel Demok: samvmdemok@gmail.com

Nancy Endersby-Harshman: nancye@unimelb.edu.au

Rebecca Vinit: rebeccavinit31@gmail.com

Lincoln Timinao: lincoln.timinao@gmail.com

Leanne J. Robinson: leanne.robinson@burnet.edu.au

Melinda Susapu: msusapu@gmail.com

Leo Makita: leo.makita@gmail.com

Moses Laman: moses.laman@pngimr.org.pg

Ary Hoffmann: ary@unimelb.edu.au

Stephan Karl: stephan.karl@jcu.edu.au

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 3 July 2019

Publication date PMC-release: 3 July 2019

Publication date Collection: 2019

Volume: 12

Electronic Location Identifier: 333

Affiliations

[1 ]ISNI 0000 0001 2288 2831, GRID grid.417153.5, Vector-Borne Diseases Unit, , PNG Institute of Medical Research, ; P.O. Box 378, Madang, 511 Madang Province Papua New Guinea

[2 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, School of BioSciences, Bio21 Institute, , The University of Melbourne, ; 30 Flemington Rd., Parkville, VIC 3010 Australia

[3 ]ISNI 0000 0004 0474 1797, GRID grid.1011.1, Australian Institute of Tropical Health and Medicine, , James Cook University, ; 1/14-88 McGregor Road, Smithfield, QLD 4870 Australia

[4 ]ISNI 0000 0001 2224 8486, GRID grid.1056.2, Burnet Institute, ; 85 Commercial Road, Melbourne, VIC 3004 Australia

[5 ]GRID grid.452626.1, National Department of Health, ; Waigani Drive, P.O. Box 807, Port Moresby, Papua New Guinea

Article

Publisher ID: 3585

DOI: 10.1186/s13071-019-3585-6

PMC ID: 6609403

PubMed ID: 31269965

SO-VID: 3f0eb27a-d6e3-4954-9491-b10c402c56ea

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 25 April 2019

Date accepted : 27 June 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;

Award ID: Career Development Fellowship GNT1141441

Award ID: Program Grant

Award Recipient : Ary Hoffmann Stephan Karl

Funded by: FundRef http://dx.doi.org/10.13039/501100001792, James Cook University;

Award ID: PhD Scholarship

Award Recipient : Lincoln Timinao

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: aedes aegypti,aedes albopictus,pyrethroid resistance,deltamethrin,papua new guinea,port moresby,madang,bioassay,insecticide

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: aedes aegypti, aedes albopictus, pyrethroid resistance, deltamethrin, papua new guinea, port moresby, madang, bioassay, insecticide

Insecticide resistance status of Aedes aegypti and Aedes albopictus mosquitoes in Papua New Guinea

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Malaria vaccine development

Most cited references 29

Pyrethroid resistance in Aedes aegypti and Aedes albopictus: Important mosquito vectors of human diseases.

Molecular evidence for dual pyrethroid-receptor sites on a mosquito sodium channel.

Insecticide Resistance Status of United States Populations of Aedes albopictus and Mechanisms Involved

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