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      Global expansion and redistribution of Aedes-borne virus transmission risk with climate change

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          Abstract

          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.

          Author summary

          The established scientific consensus indicates that climate change will severely exacerbate the risk and burden of Aedes-transmitted viruses, including dengue, chikungunya, Zika, and other significant threats to global health security. Here, we show more subtle impacts of climate change on transmission, caused primarily by differences between the more heat-tolerant Aedes aegypti and the more heat-limited Ae. albopictus. Within the next century, nearly a billion people could face their first exposure to viral transmission from either mosquito in the worst-case scenario, mainly in Europe and high-elevation tropical and subtropical regions. However, while year-round transmission potential from Ae. aegypti is likely to expand (particularly in south Asia and sub-Saharan Africa), Ae. albopictus transmission potential is likely to decline substantially in the tropics, marking a global shift towards seasonal risk as the tropics eventually become too hot for transmission by Ae. albopictus. Complete mitigation of climate change to a pre-industrial baseline may protect almost a billion people from arbovirus range expansions; however, middle-of-the-road mitigation could produce the greatest expansion in the potential for viral transmission by Ae. albopictus. In any scenario, mitigating climate change would shift the projected burden of both dengue and chikungunya (and potentially other Aedes transmitted viruses) from higher-income regions back onto the tropics, where transmission might otherwise begin to decline due to rising temperatures.

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          Most cited references61

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          Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus.

          Aedes albopictus, commonly known as the Asian tiger mosquito, is currently the most invasive mosquito in the world. It is of medical importance due to its aggressive daytime human-biting behavior and ability to vector many viruses, including dengue, LaCrosse, and West Nile. Invasions into new areas of its potential range are often initiated through the transportation of eggs via the international trade in used tires. We use a genetic algorithm, Genetic Algorithm for Rule Set Production (GARP), to determine the ecological niche of Ae. albopictus and predict a global ecological risk map for the continued spread of the species. We combine this analysis with risk due to importation of tires from infested countries and their proximity to countries that have already been invaded to develop a list of countries most at risk for future introductions and establishments. Methods used here have potential for predicting risks of future invasions of vectors or pathogens.
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            Potential effect of population and climate changes on global distribution of dengue fever: an empirical model.

            Existing theoretical models of the potential effects of climate change on vector-borne diseases do not account for social factors such as population increase, or interactions between climate variables. Our aim was to investigate the potential effects of global climate change on human health, and in particular, on the transmission of vector-borne diseases. We modelled the reported global distribution of dengue fever on the basis of vapour pressure, which is a measure of humidity. We assessed changes in the geographical limits of dengue fever transmission, and in the number of people at risk of dengue by incorporating future climate change and human population projections into our model. We showed that the current geographical limits of dengue fever transmission can be modelled with 89% accuracy on the basis of long-term average vapour pressure. In 1990, almost 30% of the world population, 1.5 billion people, lived in regions where the estimated risk of dengue transmission was greater than 50%. With population and climate change projections for 2085, we estimate that about 5-6 billion people (50-60% of the projected global population) would be at risk of dengue transmission, compared with 3.5 billion people, or 35% of the population, if climate change did not happen. We conclude that climate change is likely to increase the area of land with a climate suitable for dengue fever transmission, and that if no other contributing factors were to change, a large proportion of the human population would then be put at risk.
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              The global emergence/resurgence of arboviral diseases as public health problems.

              During the past 20 years there has been a dramatic resurgence or emergence of epidemic arboviral diseases affecting both humans and domestic animals. These epidemics have been caused primarily by viruses thought to be under control such as dengue, Japanese encephalitis, yellow fever, and Venezuelan equine encephalitis, or viruses that have expanded their geographic distribution such as West Nile and Rift Valley fever. Several of these viruses are presented as case studies to illustrate the changing epidemiology. The factors responsible for the dramatic resurgence of arboviral diseases in the waning years of the 20th century are discussed, as is the need for rebuilding the public health infrastructure to deal with epidemic vector-borne diseases in the 21st century.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Funding acquisitionRole: MethodologyRole: ResourcesRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: 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 March 2019
                March 2019
                : 13
                : 3
                : e0007213
                Affiliations
                [1 ] Department of Geography, University of Florida, Gainesville, Florida, United States of America
                [2 ] Emerging Pathogens Institute, University of Florida, Gainesville, Florida, United States of America
                [3 ] School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa
                [4 ] Department of Biology, Georgetown University, Washington, DC, United States of America
                [5 ] National Socio-Environmental Synthesis Center, University of Maryland, Annapolis, Maryland, United States of America
                [6 ] Department of Biology, Stanford University, Stanford, California, United States of America
                [7 ] Department of Statistics, Virginia Polytechnic and State University, Blacksburg, Virginia, United States of America
                Cary Institute of Ecosystem Studies, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                ‡ These authors are joint first authors on this work.

                Author information
                http://orcid.org/0000-0002-4308-6321
                Article
                PNTD-D-18-01324
                10.1371/journal.pntd.0007213
                6438455
                30921321
                24991d11-8fb7-4adf-b8bd-95eb4a66d31a
                © 2019 Ryan 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
                : 11 September 2018
                : 4 February 2019
                Page count
                Figures: 3, Tables: 3, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000076, Directorate for Biological Sciences;
                Award ID: 1518681
                Funded by: funder-id http://dx.doi.org/10.13039/100000076, Directorate for Biological Sciences;
                Award ID: 1641145
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000076, Directorate for Biological Sciences;
                Award ID: 1640780
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000030, Centers for Disease Control and Prevention;
                Award ID: 1U01CK000510-01
                Award Recipient :
                This work was funded by the National Science Foundation (DEB-1518681 to SJR, LRJ, EAM, NSF DEB-1641145 to SJR, and DEB-1640780 to EAM), and CDC grant 1U01CK000510-01: Southeastern Regional Center of Excellence in Vector-Borne Diseases: the Gateway Program, to SJR. This publication was supported by the Cooperative Agreement Number above from the Centers for Disease Control and Prevention. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the Centers for Disease Control and Prevention. Support was also provided by the Stanford Woods Institute for the Environment (https:// woods.stanford.edu/research/environmental- venture-projects), and the Stanford Center for Innovation in Global Health ( http://globalhealth. stanford.edu/research/seed-grants.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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