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      Combined sterile insect technique and incompatible insect technique: The first proof-of-concept to suppress Aedes aegypti vector populations in semi-rural settings in Thailand

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          Abstract

          Background

          Important arboviral diseases, such as dengue, chikungunya, and Zika virus infections, are transmitted mainly by the Aedes aegypti vector. So far, controlling this vector species with current tools and strategies has not demonstrated sustainable and significant impacts. Our main objective was to evaluate whether open field release of sterile males, produced from combining the sterile insect technique using radiation with the insect incompatible technique through Wolbachia-induced incompatibility (SIT/IIT), could suppress natural populations of Ae. aegypti in semi-rural village settings in Thailand.

          Methodology/Principal findings

          Irradiated Wolbachia-infected Aedes aegypti males produced by the SIT/IIT approach were completely sterile and were able to compete with the wild fertile ones. Open field release of these sterile males was conducted in an ecologically isolated village in Chachoengsao Province, eastern Thailand. House-to-house visit and media reports resulted in community acceptance and public awareness of the technology. During intervention, approximately 100–200 sterile males were released weekly in each household. After 6 months of sterile male release, a significant reduction ( p<0.05) of the mean egg hatch rate (84%) and the mean number of females per household (97.30%) was achieved in the treatment areas when compared to the control ones.

          Conclusions/Significance

          Our study represents the first open field release of sterile Ae. aegypti males developed from a combined SIT/IIT approach. Entomological assessment using ovitraps, adult sticky traps, and portable vacuum aspirators confirmed the success in reducing natural populations of Ae. aegypti females in treated areas. Public awareness through media resulted in positive support for practical use of this strategy in wider areas. Further study using a systematic randomized trial is needed to determine whether this approach could have a significant impact on the diseases transmitted by Ae. aegypti vector.

          Author summary

          Dengue, chikungunya, and Zika are important diseases that pass to humans only by the bites of Aedes aegypti mosquitoes infected with these viruses. Due to the lack of an effective vaccine and drug to cure these diseases, mosquito control is the only method available to reduce disease risk. Most of the available preventive and control measures involve an application of chemical-based products. The inappropriate use of chemicals causes insecticide resistance and environmental contamination. In this study, we report on the pilot trial of an alternative, safe, and environmental friendly approach to suppress Ae. aegypti mosquito populations. This alternative method involves the release of sterile Ae. aegypti males that were infected with, naturally-occurring, insect bacteria Wolbachia, and were irradiated at low doses to obtain full sterilization. The pilot trial involved the release of 100–200 sterile males per household in a treated area over a 6-month period. High efficacy of this approach was evidenced from a significant reduction in the numbers of wild Ae. aegypti females and an increase in sterility by reduction in the egg hatch rate of wild Ae. aegypti females in the treated area. Public awareness through media resulted in public support to conduct trials in wider areas.

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          Most cited references30

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          Suppression of a Field Population of Aedes aegypti in Brazil by Sustained Release of Transgenic Male Mosquitoes

          The increasing burden of dengue, and the relative failure of traditional vector control programs highlight the need to develop new control methods. SIT using self-limiting genetic technology is one such promising method. A self-limiting strain of Aedes aegypti, OX513A, has already reached the stage of field evaluation. Sustained releases of OX513A Ae. aegypti males led to 80% suppression of a target wild Ae. aegypti population in the Cayman Islands in 2010. Here we describe sustained series of field releases of OX513A Ae. aegypti males in a suburb of Juazeiro, Bahia, Brazil. This study spanned over a year and reduced the local Ae. aegypti population by 95% (95% CI: 92.2%-97.5%) based on adult trap data and 81% (95% CI: 74.9-85.2%) based on ovitrap indices compared to the adjacent no-release control area. The mating competitiveness of the released males (0.031; 95% CI: 0.025-0.036) was similar to that estimated in the Cayman trials (0.059; 95% CI: 0.011 – 0.210), indicating that environmental and target-strain differences had little impact on the mating success of the OX513A males. We conclude that sustained release of OX513A males may be an effective and widely useful method for suppression of the key dengue vector Ae. aegypti. The observed level of suppression would likely be sufficient to prevent dengue epidemics in the locality tested and other areas with similar or lower transmission.
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            Incompatible and sterile insect techniques combined eliminate mosquitoes

            The radiation-based sterile insect technique (SIT) has successfully suppressed field populations of several insect pest species, but its effect on mosquito vector control has been limited. The related incompatible insect technique (IIT)-which uses sterilization caused by the maternally inherited endosymbiotic bacteria Wolbachia-is a promising alternative, but can be undermined by accidental release of females infected with the same Wolbachia strain as the released males. Here we show that combining incompatible and sterile insect techniques (IIT-SIT) enables near elimination of field populations of the world's most invasive mosquito species, Aedes albopictus. Millions of factory-reared adult males with an artificial triple-Wolbachia infection were released, with prior pupal irradiation of the released mosquitoes to prevent unintentionally released triply infected females from successfully reproducing in the field. This successful field trial demonstrates the feasibility of area-wide application of combined IIT-SIT for mosquito vector control.
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              An update on Zika virus infection

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: SupervisionRole: VisualizationRole: Writing – original draft
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: InvestigationRole: Project administrationRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                28 October 2019
                October 2019
                : 13
                : 10
                : e0007771
                Affiliations
                [1 ] Center of Excellence for Vectors and Vector-Borne Diseases, Faculty of Science, Mahidol University at Salaya, Nakhon Pathom, Thailand
                [2 ] Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand
                [3 ] Thailand Institute of Nuclear Technology, Ministry of Science and Technology, Nakhon Nayok, Thailand
                [4 ] Department of Medical Sciences, Ministry of Public Health, Nonthaburi, Thailand
                [5 ] Department of Disease Control, Ministry of Public Health, Nonthaburi, Thailand
                University of Hawaii at Manoa, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-4234-1239
                Article
                PNTD-D-18-01991
                10.1371/journal.pntd.0007771
                6837763
                31658265
                34018629-500a-495c-8d79-8746964a9fb7
                © 2019 Kittayapong et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 28 December 2018
                : 10 September 2019
                Page count
                Figures: 4, Tables: 5, Pages: 21
                Funding
                Funded by: IDRC/FBLI
                Award ID: 106556
                Award Recipient :
                Funded by: IAEA/TC
                Award ID: RAS5066
                Award Recipient :
                Funded by: IAEA/CRP
                Award ID: D44002/19059
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100007180, Faculty of Science, Mahidol University;
                Award Recipient :
                This study received financial support from the International Development Research Centre (IDRC/FBLI/106556), the International Atomic Energy Agency (IAEA/TC/RAS5066 & IAEA/CRP/D44002/19059) and Mahidol University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Aedes Aegypti
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Bacteria
                Wolbachia
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Medicine and Health Sciences
                Infectious Diseases
                Infectious Disease Control
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                People and Places
                Geographical Locations
                Asia
                Thailand
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Chikungunya Infection
                Medicine and Health Sciences
                Infectious Diseases
                Viral Diseases
                Chikungunya Infection
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-11-07
                All data is available at: https://dataverse.harvard.edu/dataverse/combined-SIT-IIT-Thailand.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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