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      Re-assess Vector Indices Threshold as an Early Warning Tool for Predicting Dengue Epidemic in a Dengue Non-endemic Country

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          Abstract

          Background

          Despite dengue dynamics being driven by complex interactions between human hosts, mosquito vectors and viruses that are influenced by climate factors, an operational model that will enable health authorities to anticipate the outbreak risk in a dengue non-endemic area has not been developed. The objectives of this study were to evaluate the temporal relationship between meteorological variables, entomological surveillance indices and confirmed dengue cases; and to establish the threshold for entomological surveillance indices including three mosquito larval indices [Breteau (BI), Container (CI) and House indices (HI)] and one adult index (AI) as an early warning tool for dengue epidemic.

          Methodology/Principal Findings

          Epidemiological, entomological and meteorological data were analyzed from 2005 to 2012 in Kaohsiung City, Taiwan. The successive waves of dengue outbreaks with different magnitudes were recorded in Kaohsiung City, and involved a dominant serotype during each epidemic. The annual indigenous dengue cases usually started from May to June and reached a peak in October to November. Vector data from 2005–2012 showed that the peak of the adult mosquito population was followed by a peak in the corresponding dengue activity with a lag period of 1–2 months. Therefore, we focused the analysis on the data from May to December and the high risk district, where the inspection of the immature and mature mosquitoes was carried out on a weekly basis and about 97.9% dengue cases occurred. The two-stage model was utilized here to estimate the risk and time-lag effect of annual dengue outbreaks in Taiwan. First, Poisson regression was used to select the optimal subset of variables and time-lags for predicting the number of dengue cases, and the final results of the multivariate analysis were selected based on the smallest AIC value. Next, each vector index models with selected variables were subjected to multiple logistic regression models to examine the accuracy of predicting the occurrence of dengue cases. The results suggested that Model-AI, BI, CI and HI predicted the occurrence of dengue cases with 83.8, 87.8, 88.3 and 88.4% accuracy, respectively. The predicting threshold based on individual Model-AI, BI, CI and HI was 0.97, 1.16, 1.79 and 0.997, respectively.

          Conclusion/Significance

          There was little evidence of quantifiable association among vector indices, meteorological factors and dengue transmission that could reliably be used for outbreak prediction. Our study here provided the proof-of-concept of how to search for the optimal model and determine the threshold for dengue epidemics. Since those factors used for prediction varied, depending on the ecology and herd immunity level under different geological areas, different thresholds may be developed for different countries using a similar structure of the two-stage model.

          Author Summary

          With the continuously high levels of worldwide dengue transmission, predicting dengue outbreaks in advance of their occurrence or identifying specific locations where outbreak risks are highest is of critical importance. However, only few studies have been conducted in dengue non-endemic countries to evaluate the association of vector index with the occurrence of dengue cases; and the establishment of an early warning signal would significantly enhance the public health intervention. Our study here provided the proof-of-concept results, utilizing a two-stage model to identify the best set of lag effects of meteorological and entomological variables, explaining dengue epidemics based on the data obtained from Taiwan, which is a dengue-non-endemic country. Each of the vector indices when combined with the meteorological factors has better performance compared to the prediction using AI, BI, CI and HI alone, with 83.8, 87.8, 88.3 and 88.4% accuracy, respectively. Because of the complex interplays between the size of human hosts and movement, environmental factors and dynamic changes of mosquito population and density, each country should consider its own individual data and situation and apply this two-stage model to find the optimal predictive models for allocating public health resources and prevention strategies.

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          Most cited references48

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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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            Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti.

            Most studies on the ability of insect populations to transmit pathogens consider only constant temperatures and do not account for realistic daily temperature fluctuations that can impact vector-pathogen interactions. Here, we show that diurnal temperature range (DTR) affects two important parameters underlying dengue virus (DENV) transmission by Aedes aegypti. In two independent experiments using different DENV serotypes, mosquitoes were less susceptible to virus infection and died faster under larger DTR around the same mean temperature. Large DTR (20 °C) decreased the probability of midgut infection, but not duration of the virus extrinsic incubation period (EIP), compared with moderate DTR (10 °C) or constant temperature. A thermodynamic model predicted that at mean temperatures 18 °C, larger DTR reduces DENV transmission. The negative impact of DTR on Ae. aegypti survival indicates that large temperature fluctuations will reduce the probability of vector survival through EIP and expectation of infectious life. Seasonal variation in the amplitude of daily temperature fluctuations helps to explain seasonal forcing of DENV transmission at locations where average temperature does not vary seasonally and mosquito abundance is not associated with dengue incidence. Mosquitoes lived longer and were more likely to become infected under moderate temperature fluctuations, which is typical of the high DENV transmission season than under large temperature fluctuations, which is typical of the low DENV transmission season. Our findings reveal the importance of considering short-term temperature variations when studying DENV transmission dynamics.
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              Global Change and Human Vulnerability to Vector-Borne Diseases

              Global change includes climate change and climate variability, land use, water storage and irrigation, human population growth and urbanization, trade and travel, and chemical pollution. Impacts on vector-borne diseases, including malaria, dengue fever, infections by other arboviruses, schistosomiasis, trypanosomiasis, onchocerciasis, and leishmaniasis are reviewed. While climate change is global in nature and poses unknown future risks to humans and natural ecosystems, other local changes are occurring more rapidly on a global scale and are having significant effects on vector-borne diseases. History is invaluable as a pointer to future risks, but direct extrapolation is no longer possible because the climate is changing. Researchers are therefore embracing computer simulation models and global change scenarios to explore the risks. Credible ranking of the extent to which different vector-borne diseases will be affected awaits a rigorous analysis. Adaptation to the changes is threatened by the ongoing loss of drugs and pesticides due to the selection of resistant strains of pathogens and vectors. The vulnerability of communities to the changes in impacts depends on their adaptive capacity, which requires both appropriate technology and responsive public health systems. The availability of resources in turn depends on social stability, economic wealth, and priority allocation of resources to public health.
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                Author and article information

                Contributors
                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
                14 September 2015
                September 2015
                : 9
                : 9
                : e0004043
                Affiliations
                [1 ]Graduate Institute of Microbiology and Public Health, College of Veterinary Medicine, National Chung-Hsing University, Taichung, Taiwan
                [2 ]Graduate Institute of Statistics and Information Science, National Changhua University of Education, Changhua, Taiwan
                [3 ]Department of Family Medicine, Taichung Hospital, Department of Health, Executive Yuan, Taiwan, R.O.C
                [4 ]Department of Health, Kaohsiung City Government, Kaohsiung City, Taiwan
                Santa Fe Institute, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: IBL DYC. Performed the experiments: FSC YTT. Analyzed the data: FSC DYC YTT. Contributed reagents/materials/analysis tools: PSH CDC IBL. Wrote the paper: IBL DYC.

                Article
                PNTD-D-15-00635
                10.1371/journal.pntd.0004043
                4569482
                26366874
                f27c5738-cc9f-4751-94ba-7ae816fd70ae
                Copyright @ 2015

                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
                : 15 April 2015
                : 9 August 2015
                Page count
                Figures: 4, Tables: 3, Pages: 20
                Funding
                The funding support for DYC and IBL was provided by Ministry of Science and Technology-Taiwan (NSC101-2923-B-005-001-MY3, NSC102-2627-M-005-004). The funder website is http://www.most.gov.tw/. The funder had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Data are available from the Taichung Hospital, Ministry of Health and Welfare, Institutional Data Access / Ethics Committee for researchers who meet the criteria for access to confidential data. The contact email and phone number is taic89384@ 123456taic.mohw.gov.tw and 886-4-22294411 ext 5429.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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