Establishment of
 w Mel
 Wolbachia  in
 Aedes aegypti  mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia

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Abstract

Background: The wMel strain of Wolbachia has been successfully introduced into Aedes aegypti mosquitoes and subsequently shown in laboratory studies to reduce transmission of a range of viruses including dengue, Zika, chikungunya, yellow fever, and Mayaro viruses that cause human disease. Here we report the entomological and epidemiological outcomes of staged deployment of Wolbachia across nearly all significant dengue transmission risk areas in Australia.

Methods: The wMel strain of Wolbachia was backcrossed into the local Aedes aegypti genotype (Cairns and Townsville backgrounds) and mosquitoes were released in the field by staff or via community assisted methods. Mosquito monitoring was undertaken and mosquitoes were screened for the presence of Wolbachia. Dengue case notifications were used to track dengue incidence in each location before and after releases.

Results: Empirical analyses of the Wolbachia mosquito releases, including data on the density, frequency and duration of Wolbachia mosquito releases, indicate that Wolbachia can be readily established in local mosquito populations, using a variety of deployment options and over short release durations (mean release period 11 weeks, range 2-22 weeks). Importantly, Wolbachia frequencies have remained stable in mosquito populations since releases for up to 8 years. Analysis of dengue case notifications data demonstrates near-elimination of local dengue transmission for the past five years in locations where Wolbachia has been established. The regression model estimate of Wolbachia intervention effect from interrupted time series analyses of case notifications data prior to and after releases, indicated a 96% reduction in dengue incidence in Wolbachia treated populations (95% confidence interval: 84 – 99%).

Conclusion: Deployment of the wMel strain of Wolbachia into local Ae. aegypti populations across the Australian regional cities of Cairns and most smaller regional communities with a past history of dengue has resulted in the reduction of local dengue transmission across all deployment areas.

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Most cited references 33

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A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium.

Luciano Moreira, Inaki Iturbe-Ormaetxe, Jason Jeffery … (2009)

Wolbachia are maternally inherited intracellular bacterial symbionts that are estimated to infect more than 60% of all insect species. While Wolbachia is commonly found in many mosquitoes it is absent from the species that are considered to be of major importance for the transmission of human pathogens. The successful introduction of a life-shortening strain of Wolbachia into the dengue vector Aedes aegypti that halves adult lifespan has recently been reported. Here we show that this same Wolbachia infection also directly inhibits the ability of a range of pathogens to infect this mosquito species. The effect is Wolbachia strain specific and relates to Wolbachia priming of the mosquito innate immune system and potentially competition for limiting cellular resources required for pathogen replication. We suggest that this Wolbachia-mediated pathogen interference may work synergistically with the life-shortening strategy proposed previously to provide a powerful approach for the control of insect transmitted diseases. Copyright 2009 Elsevier Inc. All rights reserved.

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Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission.

A Hoffmann, B. L. Montgomery, J Popovici … (2011)

Genetic manipulations of insect populations for pest control have been advocated for some time, but there are few cases where manipulated individuals have been released in the field and no cases where they have successfully invaded target populations. Population transformation using the intracellular bacterium Wolbachia is particularly attractive because this maternally-inherited agent provides a powerful mechanism to invade natural populations through cytoplasmic incompatibility. When Wolbachia are introduced into mosquitoes, they interfere with pathogen transmission and influence key life history traits such as lifespan. Here we describe how the wMel Wolbachia infection, introduced into the dengue vector Aedes aegypti from Drosophila melanogaster, successfully invaded two natural A. aegypti populations in Australia, reaching near-fixation in a few months following releases of wMel-infected A. aegypti adults. Models with plausible parameter values indicate that Wolbachia-infected mosquitoes suffered relatively small fitness costs, leading to an unstable equilibrium frequency <30% that must be exceeded for invasion. These findings demonstrate that Wolbachia-based strategies can be deployed as a practical approach to dengue suppression with potential for area-wide implementation.

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The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations.

Woolf Walker, Francesca D. Frentiu, Conor McMeniman … (2011)

Dengue fever is the most important mosquito-borne viral disease of humans with more than 50 million cases estimated annually in more than 100 countries. Disturbingly, the geographic range of dengue is currently expanding and the severity of outbreaks is increasing. Control options for dengue are very limited and currently focus on reducing population abundance of the major mosquito vector, Aedes aegypti. These strategies are failing to reduce dengue incidence in tropical communities and there is an urgent need for effective alternatives. It has been proposed that endosymbiotic bacterial Wolbachia infections of insects might be used in novel strategies for dengue control. For example, the wMelPop-CLA Wolbachia strain reduces the lifespan of adult A. aegypti mosquitoes in stably transinfected lines. This life-shortening phenotype was predicted to reduce the potential for dengue transmission. The recent discovery that several Wolbachia infections, including wMelPop-CLA, can also directly influence the susceptibility of insects to infection with a range of insect and human pathogens has markedly changed the potential for Wolbachia infections to control human diseases. Here we describe the successful transinfection of A. aegypti with the avirulent wMel strain of Wolbachia, which induces the reproductive phenotype cytoplasmic incompatibility with minimal apparent fitness costs and high maternal transmission, providing optimal phenotypic effects for invasion. Under semi-field conditions, the wMel strain increased from an initial starting frequency of 0.65 to near fixation within a few generations, invading A. aegypti populations at an accelerated rate relative to trials with the wMelPop-CLA strain. We also show that wMel and wMelPop-CLA strains block transmission of dengue serotype 2 (DENV-2) in A. aegypti, forming the basis of a practical approach to dengue suppression.

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Author and article information

Contributors

Peter A. Ryan: Role: ConceptualizationRole: Formal AnalysisRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – Original Draft PreparationRole: Writing – Review & Editing

ORCID: https://orcid.org/0000-0003-0674-4441

Andrew P. Turley: Role: MethodologyRole: Project AdministrationRole: SupervisionRole: Writing – Review & Editing

Geoff Wilson: Role: InvestigationRole: MethodologyRole: Project AdministrationRole: SupervisionRole: Writing – Review & Editing

Tim P. Hurst: Role: InvestigationRole: Project AdministrationRole: SupervisionRole: Writing – Review & Editing

Kate Retzki: Role: InvestigationRole: MethodologyRole: Project AdministrationRole: Writing – Review & Editing

Jack Brown-Kenyon: Role: Data CurationRole: Formal AnalysisRole: ValidationRole: VisualizationRole: Writing – Review & Editing

Lauren Hodgson: Role: Data CurationRole: Formal AnalysisRole: Project AdministrationRole: ValidationRole: VisualizationRole: Writing – Review & Editing

Nichola Kenny: Role: InvestigationRole: MethodologyRole: SupervisionRole: Writing – Review & Editing

Helen Cook: Role: InvestigationRole: MethodologyRole: Writing – Review & Editing

Brian L. Montgomery: Role: InvestigationRole: MethodologyRole: Project AdministrationRole: SupervisionRole: Writing – Review & Editing

Christopher J. Paton: Role: InvestigationRole: MethodologyRole: Writing – Review & Editing

Scott A. Ritchie: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – Review & Editing

Ary A. Hoffmann: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – Review & Editing

Nicholas P. Jewell: Role: Formal AnalysisRole: MethodologyRole: Writing – Review & Editing

Stephanie K. Tanamas: Role: Formal AnalysisRole: MethodologyRole: Writing – Review & Editing

Katherine L. Anders: Role: ConceptualizationRole: Formal AnalysisRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – Original Draft PreparationRole: Writing – Review & Editing

ORCID: https://orcid.org/0000-0003-0485-5826

Cameron P. Simmons: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – Review & Editing

Scott L. O’Neill: Role: ConceptualizationRole: Formal AnalysisRole: Funding AcquisitionRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – Original Draft PreparationRole: Writing – Review & Editing

ORCID: https://orcid.org/0000-0002-4131-3615

Journal

Journal ID (nlm-ta): Gates Open Res

Journal ID (iso-abbrev): Gates Open Res

Journal ID (pmc): Gates Open Res

Title: Gates Open Research

Publisher: F1000 Research Limited (London, UK )

ISSN (Electronic): 2572-4754

Publication date (Electronic): 26 September 2019

Publication date Collection: 2019

Volume: 3

Electronic Location Identifier: 1547

Affiliations

[1 ]Institute of Vector-Borne Disease, Monash University, Clayton, Victoria, 3800, Australia

[2 ]Biosecurity and Agricultural Services, Department of Jobs, Precincts and Regions, Victoria State Government, Atwood, Victoria, Australia

[3 ]Metro South Public Health Unit, Queensland Health, Coopers Plains, Queensland, Australia

[4 ]College of Public Health, Medical and Veterinary Sciences, James Cook University, Cairns, Queensland, Australia

[5 ]School of Biosciences, Bio21 Institute, University of Melbourne, Parkville, Victoria, Australia

[6 ]Division of Epidemiology and Biostatistics, School of Public Health, University of California, Berkeley, California, USA

[7 ]Centre for Statistical Methodology, London School of Hygiene and Tropical Medicine, London, UK

[8 ]Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam

[1 ]Department of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, UK

[1 ]Yale University, New Haven, CT, USA

Author notes

[a ] scott.oneill@ 123456worldmosquito.org

No competing interests were disclosed.

Competing interests: No competing interests were disclosed.

Author information

Peter A. Ryan https://orcid.org/0000-0003-0674-4441

Katherine L. Anders https://orcid.org/0000-0003-0485-5826

Scott L. O’Neill https://orcid.org/0000-0002-4131-3615

Article

DOI: 10.12688/gatesopenres.13061.1

PMC ID: 6801363

PubMed ID: 31667465

SO-VID: 6f879610-606b-40ec-8246-0124f73df67d

License:

This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date accepted : 18 September 2019

Funding

Funded by: Gillespie Foundation

Funded by: Bill and Melinda Gates Foundation

Award ID: OPP1180815

Award ID: OPP1153619

Funded by: Queensland Government

Award ID: 70134

Funded by: National Health and Medical Research Council

Award ID: 1132412

Funded by: National Health and Medical Research Council

Award ID: 1037003

Funded by: National Health and Medical Research Council

Award ID: 1118640

Funded by: National Health and Medical Research Council

Award ID: 1044698

Funded by: Wellcome Trust

Award ID: 102591

This work was supported by the Bill and Melinda Gates Foundation [OPP1180815] and through a grant as part the Vector-Based Transmission of Control: Discovery Research (VCTR) program of the Grand Challenges in Global Health initiative [OPP1153619] managed by the Foundation for the National Institutes of Health. This work was also supported by the Wellcome Trust [102591], National Health and Medical Research Council of Australia Program Grants [1037003 and 1132412], the Queensland Government [Project ID 70134], and the Gillespie Family Foundation. SAR and AAH were funded from the National Health and Medical Research Council of Australia through Research Fellowship awards [1044698 and 1118640, respectively].

The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Establishment of wMel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia

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Zika Virus

Most cited references 33

A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium.

Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission.

The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations.

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