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      Local and Global Effects of Climate on Dengue Transmission in Puerto Rico

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          Abstract

          The four dengue viruses, the agents of dengue fever and dengue hemorrhagic fever in humans, are transmitted predominantly by the mosquito Aedes aegypti. The abundance and the transmission potential of Ae. aegypti are influenced by temperature and precipitation. While there is strong biological evidence for these effects, empirical studies of the relationship between climate and dengue incidence in human populations are potentially confounded by seasonal covariation and spatial heterogeneity. Using 20 years of data and a statistical approach to control for seasonality, we show a positive and statistically significant association between monthly changes in temperature and precipitation and monthly changes in dengue transmission in Puerto Rico. We also found that the strength of this association varies spatially, that this variation is associated with differences in local climate, and that this relationship is consistent with laboratory studies of the impacts of these factors on vector survival and viral replication. These results suggest the importance of temperature and precipitation in the transmission of dengue viruses and suggest a reason for their spatial heterogeneity. Thus, while dengue transmission may have a general system, its manifestation on a local scale may differ from global expectations.

          Author Summary

          Dengue viruses are a major health problem throughout the tropical and subtropical regions of the world. Because they are transmitted by mosquitoes that are sensitive to changes in rainfall and temperature, transmission intensity may be regulated by weather and climate. Laboratory studies have shown this to be biologically plausible, but studies of transmission in real-life situations have been inconclusive. Here we demonstrate that increased temperature and rainfall are associated with increased dengue transmission in subsequent months across Puerto Rico. We also show that differences in local climate within Puerto Rico can explain local differences observed in the relationship between weather and dengue transmission. This finding is important because it suggests that the determinants of transmission occur on a local level such that although dengue viruses have a basically universal transmission cycle, changes in temperature or rainfall may have diverse local effects.

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          Most cited references45

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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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            Ecological and immunological determinants of dengue epidemics.

            The management of infectious diseases is an increasingly important public health issue, the effective implementation of which is often complicated by difficulties in teasing apart the relative roles of extrinsic and intrinsic factors influencing transmission. Dengue, a vector-borne strain polymorphic disease, is one such infection where transmission dynamics are affected by environmental variables as well as immune-mediated serotype interactions. To understand how alternative hypotheses concerning dengue infection and transmission may explain observed multiannual cycles in disease incidence, we adopt a theoretical approach that combines both ecological and immunological mechanisms. We demonstrate that, contrary to perceived wisdom, patterns generated solely by antibody-dependent enhancement or heterogeneity in virus virulence are not consistent with serotype-specific notification data in important ways. Furthermore, to generate epidemics with the characteristic signatures observed in data, we find that a combination of seasonal variation in vector demography and, crucially, a short-lived period of cross-immunity is sufficient. We then show how understanding the persistence and eradication of dengue serotypes critically depends on the alternative assumed mechanisms.
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              Effect of temperature on the vector efficiency of Aedes aegypti for dengue 2 virus.

              The effect of temperature on the ability of Aedes aegypti to transmit dengue (DEN) 2 virus to rhesus monkeys was assessed as a possible explanation for the seasonal variation in the incidence of dengue hemorrhagic fever in Bangkok, Thailand. In two laboratory experiments, a Bangkok strain of Ae. aegypti was allowed to feed upon viremic monkeys infected with DEN-2 virus. Blood-engorged mosquitoes were separated into two groups and retained at constant temperatures. Virus infection and transmission rates were determined for Ae. aegypti at intervals ranging from 4 to 7 days during a 25-day incubation period. Results of the first experiment for mosquitoes infected with a low dose of DEN-2 virus and maintained at 20, 24, 26, and 30 degrees C, indicated that the infection rate ranged from 25% to 75% depending on the incubation period. However, DEN-2 virus was transmitted to monkeys only by Ae. aegypti retained at 30 degrees C for 25 days. In the second experiment, the infection rate for Ae. aegypti that ingested a higher viral dose, and incubated at 26, 30, 32, and 35 degrees C ranged from 67% to 95%. DEN-2 virus was transmitted to monkeys only by mosquitoes maintained at greater than or equal to 30 degrees C. The extrinsic incubation period was 12 days for mosquitoes at 30 degrees C, and was reduced to 7 days for mosquitoes incubated at 32 degrees C and 35 degrees C. These results imply that temperature-induced variations in the vector efficiency of Ae. aegypti may be a significant determinant in the annual cyclic pattern of dengue hemorrhagic fever epidemics in Bangkok.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                February 2009
                17 February 2009
                : 3
                : 2
                : e382
                Affiliations
                [1 ]Dengue Branch, Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, San Juan, Puerto Rico, United States of America
                [2 ]W. Harry Feinstone Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
                [3 ]Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
                University of São Paulo, Brazil
                Author notes

                Conceived and designed the experiments: MAJ FD GEG. Performed the experiments: MAJ. Analyzed the data: MAJ. Contributed reagents/materials/analysis tools: FD. Wrote the paper: MAJ. Revised the paper: FD GEG.

                Article
                08-PNTD-RA-0366R2
                10.1371/journal.pntd.0000382
                2637540
                19221592
                31b09121-ee18-4a8c-af8e-9e5040e93d26
                This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                History
                : 10 October 2008
                : 21 January 2009
                Page count
                Pages: 5
                Categories
                Research Article
                Ecology/Ecosystem Ecology
                Ecology/Spatial and Landscape Ecology
                Infectious Diseases/Neglected Tropical Diseases
                Infectious Diseases/Viral Infections
                Mathematics/Statistics
                Public Health and Epidemiology/Epidemiology
                Public Health and Epidemiology/Global Health
                Public Health and Epidemiology/Infectious Diseases

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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