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      Effectiveness of Wolbachia-infected mosquito deployments in reducing the incidence of dengue and other Aedes-borne diseases in Niterói, Brazil: A quasi-experimental study

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          Abstract

          Background

          The introduction of the bacterium Wolbachia ( wMel strain) into Aedes aegypti mosquitoes reduces their capacity to transmit dengue and other arboviruses. Evidence of a reduction in dengue case incidence following field releases of wMel-infected Ae. aegypti has been reported previously from a cluster randomised controlled trial in Indonesia, and quasi-experimental studies in Indonesia and northern Australia.

          Methodology/Principal findings

          Following pilot releases in 2015–2016 and a period of intensive community engagement, deployments of adult wMel-infected Ae. aegypti mosquitoes were conducted in Niterói, Brazil during 2017–2019. Deployments were phased across four release zones, with a total area of 83 km 2 and a residential population of approximately 373,000. A quasi-experimental design was used to evaluate the effectiveness of wMel deployments in reducing dengue, chikungunya and Zika incidence. An untreated control zone was pre-defined, which was comparable to the intervention area in historical dengue trends. The wMel intervention effect was estimated by controlled interrupted time series analysis of monthly dengue, chikungunya and Zika case notifications to the public health surveillance system before, during and after releases, from release zones and the control zone. Three years after commencement of releases, wMel introgression into local Ae. aegypti populations was heterogeneous throughout Niterói, reaching a high prevalence (>80%) in the earliest release zone, and more moderate levels (prevalence 40–70%) elsewhere. Despite this spatial heterogeneity in entomological outcomes, the wMel intervention was associated with a 69% reduction in dengue incidence (95% confidence interval 54%, 79%), a 56% reduction in chikungunya incidence (95%CI 16%, 77%) and a 37% reduction in Zika incidence (95%CI 1%, 60%), in the aggregate release area compared with the pre-defined control area. This significant intervention effect on dengue was replicated across all four release zones, and in three of four zones for chikungunya, though not in individual release zones for Zika.

          Conclusions/Significance

          We demonstrate that wMel Wolbachia can be successfully introgressed into Ae. aegypti populations in a large and complex urban setting, and that a significant public health benefit from reduced incidence of Aedes-borne disease accrues even where the prevalence of wMel in local mosquito populations is moderate and spatially heterogeneous. These findings are consistent with the results of randomised and non-randomised field trials in Indonesia and northern Australia, and are supportive of the Wolbachia biocontrol method as a multivalent intervention against dengue, chikungunya and Zika.

          Author summary

          The Aedes aegypti mosquito transmits dengue, chikungunya, Zika and other viral diseases between humans. Previous research has shown that when a symbiotic bacterium called Wolbachia–which exists naturally in many other insect species–is introduced into Ae. aegypti mosquitoes it makes them less able to transmit dengue and other viruses, and is passed from generation to generation via mosquito eggs. The authors report that after releasing Wolbachia-carrying Ae. aegypti in the Brazilian city of Niterói for periods during 2017 to 2019, between 33% and 90% of the Ae. aegypti mosquito population in four release zones were infected with Wolbachia by March 2020. The authors used controlled interrupted time series analysis to show that Wolbachia deployments were associated with a 69% reduction in dengue cases notified to the public health authorities, compared to a control area of Niterói that did not receive Wolbachia releases. Chikungunya and Zika case incidence was also significantly lower in the Wolbachia release areas. These results support previous findings from Indonesia and Australia, and show that Wolbachia mosquito releases are an effective and sustainable method for controlling dengue and other diseases spread by Ae. aegypti mosquitoes, even in large and complex urban environments.

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          Most cited references34

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          Interrupted time series regression for the evaluation of public health interventions: a tutorial

          Abstract Interrupted time series (ITS) analysis is a valuable study design for evaluating the effectiveness of population-level health interventions that have been implemented at a clearly defined point in time. It is increasingly being used to evaluate the effectiveness of interventions ranging from clinical therapy to national public health legislation. Whereas the design shares many properties of regression-based approaches in other epidemiological studies, there are a range of unique features of time series data that require additional methodological considerations. In this tutorial we use a worked example to demonstrate a robust approach to ITS analysis using segmented regression. We begin by describing the design and considering when ITS is an appropriate design choice. We then discuss the essential, yet often omitted, step of proposing the impact model a priori. Subsequently, we demonstrate the approach to statistical analysis including the main segmented regression model. Finally we describe the main methodological issues associated with ITS analysis: over-dispersion of time series data, autocorrelation, adjusting for seasonal trends and controlling for time-varying confounders, and we also outline some of the more complex design adaptations that can be used to strengthen the basic ITS design.
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            A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium.

            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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              The global burden of dengue: an analysis from the Global Burden of Disease Study 2013.

              Dengue is the most common arbovirus infection globally, but its burden is poorly quantified. We estimated dengue mortality, incidence, and burden for the Global Burden of Disease Study 2013.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: VisualizationRole: Writing – original draft
                Role: ConceptualizationRole: InvestigationRole: Methodology
                Role: InvestigationRole: SupervisionRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: Project administrationRole: Visualization
                Role: Investigation
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – review & editing
                Role: Formal analysisRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: Project administration
                Role: InvestigationRole: MethodologyRole: Project administration
                Role: InvestigationRole: MethodologyRole: Project administration
                Role: Data curationRole: InvestigationRole: MethodologyRole: Software
                Role: InvestigationRole: Methodology
                Role: MethodologyRole: Project administrationRole: Resources
                Role: MethodologyRole: Project administrationRole: Resources
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Data curationRole: Formal analysisRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draft
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                12 July 2021
                July 2021
                : 15
                : 7
                : e0009556
                Affiliations
                [1 ] World Mosquito Program, Fiocruz, Rio de Janeiro, Brazil
                [2 ] Gabinete da Presidência, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil
                [3 ] World Mosquito Program, Institute of Vector Borne Disease, Monash University, Clayton, Australia
                [4 ] Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam
                [5 ] Division of Biostatistics, School of Public Health, University of California, Berkeley, California, United States of America
                [6 ] City Health Secretariat, Niteroi, Brazil
                [7 ] City Health Secretariat, Rio de Janeiro, Brazil
                [8 ] Centre for Strategic Studies, Fiocruz, Rio de Janeiro, Brazil
                [9 ] Instituto Rene Rachou, Fiocruz, Belo Horizonte, Brazil
                University of Glasgow, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interest exist.

                Author information
                https://orcid.org/0000-0001-7758-6706
                https://orcid.org/0000-0001-7553-243X
                https://orcid.org/0000-0002-8195-6666
                https://orcid.org/0000-0002-6316-6548
                https://orcid.org/0000-0003-0674-4441
                https://orcid.org/0000-0002-4131-3615
                https://orcid.org/0000-0002-5297-4435
                https://orcid.org/0000-0003-3404-9024
                https://orcid.org/0000-0001-7360-6490
                https://orcid.org/0000-0003-0485-5826
                Article
                PNTD-D-21-00140
                10.1371/journal.pntd.0009556
                8297942
                34252106
                a52557c0-cddb-42bb-a857-3f9b52cfde1c
                © 2021 Pinto 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
                : 31 January 2021
                : 9 June 2021
                Page count
                Figures: 9, Tables: 1, Pages: 23
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100002425, Governo Brasil;
                Award ID: 25380.000814/2016-13
                Award Recipient :
                Funded by: Foundation for the National Institutes of Health through the Vector-Based Control of Transmission Discovery Research (VCTR) program of the Grand Challenges in Global Health Initiatives of the Bill and Melinda Gates Foundation
                Award ID: OPP1159497
                This work was supported by the Brazilian Ministry of Health (DECIT/SVS, grant 25380.000814/2016-13 to LAM), and a grant (OPP1159497) to Monash University from the Foundation for the National Institutes of Health through the Vector-Based Control of Transmission Discovery Research (VCTR) program of the Grand Challenges in Global Health Initiatives of the Bill and Melinda Gates Foundation. 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
                Medical Conditions
                Tropical Diseases
                Neglected Tropical Diseases
                Dengue Fever
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Viral Diseases
                Dengue Fever
                Medicine and Health Sciences
                Epidemiology
                Biology and Life Sciences
                Organisms
                Bacteria
                Wolbachia
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                Invertebrates
                Arthropoda
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                Medicine and Health Sciences
                Medical Conditions
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                Chikungunya Infection
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                Medical Conditions
                Infectious Diseases
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                Infectious Diseases
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                Custom metadata
                vor-update-to-uncorrected-proof
                2021-07-22
                Zone-level entomological and arboviral disease notification data are available at https://doi.org/10.6084/m9.figshare.13662203.v3. Neighbourhood-level entomological and dengue case notification data are available at https://doi.org/10.6084/m9.figshare.13662230.v2.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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