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      Past and future epidemic potential of chikungunya virus in Australia

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          Abstract

          Background

          Australia is theoretically at risk of epidemic chikungunya virus (CHIKV) activity as the principal vectors are present on the mainland Aedes aegypti) and some islands of the Torres Strait ( Ae. aegypti and Ae. albopictus). Both vectors are highly invasive and adapted to urban environments with a capacity to expand their distributions into south-east Queensland and other states in Australia. We sought to estimate the epidemic potential of CHIKV, which is not currently endemic in Australia, by considering exclusively transmission by the established vector in Australia, Ae. aegypti, due to the historical relevance and anthropophilic nature of the vector.

          Methodology/Principal findings

          We estimated the historical (1995–2019) epidemic potential of CHIKV in eleven Australian locations, including the Torres Strait, using a basic reproduction number equation. We found that the main urban centres of Northern Australia could sustain an epidemic of CHIKV. We then estimated future trends in epidemic potential for the main centres for the years 2020 to 2029. We also conducted uncertainty and sensitivity analyses on the variables comprising the basic reproduction number and found high sensitivity to mosquito population size, human population size, impact of vector control and human infectious period.

          Conclusions/Significance

          By estimating the epidemic potential for CHIKV transmission on mainland Australia and the Torres Strait, we identified key areas of focus for controlling vector populations and reducing human exposure. As the epidemic potential of the virus is estimated to rise towards 2029, a greater focus on control and prevention measures should be implemented in at-risk locations.

          Author summary

          Chikungunya virus (CHIKV) is transmitted primarily by Aedes aegypti and Aedes albopictus mosquitoes and causes a potentially debilitating febrile and arthralgic disease. The virus is a threat to public health in regions where the primary vectors are established, as evidenced by past epidemics in the Indian Ocean Islands, South America and the Caribbean. In Australia, there are established populations of Ae. aegypti both on the mainland and in the Torres Strait, and of Ae. albopictus in the Torres Strait. This provides a theoretical potential for CHIKV transmission, as seen historically with dengue virus (DENV). It is therefore important to understand the epidemic potential of CHIKV in Australia. We estimated the basic reproduction number ( R 0 ) of CHIKV during the years 1995–2019 for 11 Urban Centres and Localities (UCLs) in Australia, and found that Brisbane, Cairns, Darwin, Rockhampton, Thursday Island, and Townsville were all susceptible to CHIKV epidemics. We then forecasted epidemic potential from 2020–2029 and found an increase in R 0 across the six main UCLs. By highlighting factors that significantly influence the epidemic potential of CHIKV in Australia, our study supports evidence-based decision making for vector control and public health programs.

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          Most cited references50

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          A methodology for performing global uncertainty and sensitivity analysis in systems biology.

          Accuracy of results from mathematical and computer models of biological systems is often complicated by the presence of uncertainties in experimental data that are used to estimate parameter values. Current mathematical modeling approaches typically use either single-parameter or local sensitivity analyses. However, these methods do not accurately assess uncertainty and sensitivity in the system as, by default, they hold all other parameters fixed at baseline values. Using techniques described within we demonstrate how a multi-dimensional parameter space can be studied globally so all uncertainties can be identified. Further, uncertainty and sensitivity analysis techniques can help to identify and ultimately control uncertainties. In this work we develop methods for applying existing analytical tools to perform analyses on a variety of mathematical and computer models. We compare two specific types of global sensitivity analysis indexes that have proven to be among the most robust and efficient. Through familiar and new examples of mathematical and computer models, we provide a complete methodology for performing these analyses, in both deterministic and stochastic settings, and propose novel techniques to handle problems encountered during these types of analyses.
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            Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models

            Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand the seasonal and geographic range of transmission by Aedes aegypti and Ae. albopictus mosquitoes. We use mechanistic transmission models to derive predictions for how the probability and magnitude of transmission for Zika, chikungunya, and dengue change with mean temperature, and we show that these predictions are well matched by human case data. Across all three viruses, models and human case data both show that transmission occurs between 18–34°C with maximal transmission occurring in a range from 26–29°C. Controlling for population size and two socioeconomic factors, temperature-dependent transmission based on our mechanistic model is an important predictor of human transmission occurrence and incidence. Risk maps indicate that tropical and subtropical regions are suitable for extended seasonal or year-round transmission, but transmission in temperate areas is limited to at most three months per year even if vectors are present. Such brief transmission windows limit the likelihood of major epidemics following disease introduction in temperate zones.
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              Global expansion and redistribution of Aedes -borne virus transmission risk with climate change

              Forecasting the impacts of climate change on Aedes-borne viruses—especially dengue, chikungunya, and Zika—is a key component of public health preparedness. We apply an empirically parameterized model of viral transmission by the vectors Aedes aegypti and Ae. albopictus, as a function of temperature, to predict cumulative monthly global transmission risk in current climates, and compare them with projected risk in 2050 and 2080 based on general circulation models (GCMs). Our results show that if mosquito range shifts track optimal temperature ranges for transmission (21.3–34.0°C for Ae. aegypti; 19.9–29.4°C for Ae. albopictus), we can expect poleward shifts in Aedes-borne virus distributions. However, the differing thermal niches of the two vectors produce different patterns of shifts under climate change. More severe climate change scenarios produce larger population exposures to transmission by Ae. aegypti, but not by Ae. albopictus in the most extreme cases. Climate-driven risk of transmission from both mosquitoes will increase substantially, even in the short term, for most of Europe. In contrast, significant reductions in climate suitability are expected for Ae. albopictus, most noticeably in southeast Asia and west Africa. Within the next century, nearly a billion people are threatened with new exposure to virus transmission by both Aedes spp. in the worst-case scenario. As major net losses in year-round transmission risk are predicted for Ae. albopictus, we project a global shift towards more seasonal risk across regions. Many other complicating factors (like mosquito range limits and viral evolution) exist, but overall our results indicate that while climate change will lead to increased net and new exposures to Aedes-borne viruses, the most extreme increases in Ae. albopictus transmission are predicted to occur at intermediate climate change scenarios.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Investigation
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: MethodologyRole: Writing – review & editing
                Role: Investigation
                Role: ConceptualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: VisualizationRole: Writing – review & editing
                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
                16 November 2021
                November 2021
                : 15
                : 11
                : e0009963
                Affiliations
                [1 ] Centre for Immunology and Infection Control, School of Biomedical Sciences, Queensland University of Technology, Kelvin Grove, Queensland, Australia
                [2 ] Research and Development, Australian Red Cross Lifeblood, Kelvin Grove, Queensland, Australia
                [3 ] Research and Innovation Services, University of South Australia, Adelaide, South Australia, Australia
                [4 ] Metro South Public Health Unit, Metro South Hospital and Health Service, Brisbane, Queensland, Australia
                [5 ] Communicable Diseases Branch, Queensland Department of Health, Herston, Queensland, Australia
                [6 ] UniSA Clinical & Health Sciences, University of South Australia, Adelaide, South Australia, Australia
                [7 ] School of Health and Behavioural Sciences, University of the Sunshine Coast, Petrie, Queensland, Australia
                University of California, Davis, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-7755-9852
                https://orcid.org/0000-0003-2337-4753
                https://orcid.org/0000-0002-8707-6694
                https://orcid.org/0000-0002-4758-1506
                https://orcid.org/0000-0002-7257-1844
                https://orcid.org/0000-0002-3446-8248
                https://orcid.org/0000-0001-8628-4216
                https://orcid.org/0000-0002-1418-1426
                Article
                PNTD-D-20-01359
                10.1371/journal.pntd.0009963
                8631637
                34784371
                cf56149e-b6c7-47e8-8cb5-910f269ac3e0
                © 2021 White 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
                : 30 July 2020
                : 2 November 2021
                Page count
                Figures: 4, Tables: 1, Pages: 17
                Funding
                The author(s) received no specific funding for this work.
                Categories
                Research Article
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
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                Pathogens
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                Togaviruses
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                Aedes Aegypti
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                Species Interactions
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                Custom metadata
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                2021-11-30
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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