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      Climate and the Timing of Imported Cases as Determinants of the Dengue Outbreak in Guangzhou, 2014: Evidence from a Mathematical Model

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          Abstract

          As the world’s fastest spreading vector-borne disease, dengue was estimated to infect more than 390 million people in 2010, a 30-fold increase in the past half century. Although considered to be a non-endemic country, mainland China had 55,114 reported dengue cases from 2005 to 2014, of which 47,056 occurred in 2014. Furthermore, 94% of the indigenous cases in this time period were reported in Guangdong Province, 83% of which were in Guangzhou City. In order to determine the possible determinants of the unprecedented outbreak in 2014, a population-based deterministic model was developed to describe dengue transmission dynamics in Guangzhou. Regional sensitivity analysis (RSA) was adopted to calibrate the model and entomological surveillance data was used to validate the mosquito submodel. Different scenarios were created to investigate the roles of the timing of an imported case, climate, vertical transmission from mosquitoes to their offspring, and intervention. The results suggested that an early imported case was the most important factor in determining the 2014 outbreak characteristics. Precipitation and temperature can also change the transmission dynamics. Extraordinary high precipitation in May and August, 2014 appears to have increased vector abundance. Considering the relatively small number of cases in 2013, the effect of vertical transmission was less important. The earlier and more frequent intervention in 2014 also appeared to be effective. If the intervention in 2014 was the same as that in 2013, the outbreak size may have been over an order of magnitude higher than the observed number of new cases in 2014.The early date of the first imported and locally transmitted case was largely responsible for the outbreak in 2014, but it was influenced by intervention, climate and vertical transmission. Early detection and response to imported cases in the spring and early summer is crucial to avoid large outbreaks in the future.

          Author Summary

          Dengue has not been considered to be a major problem in China since it is recognized as an imported disease and only 8,058 cases were reported from 2005 to 2013. However, in 2014 alone, 47,056 new cases were reported. In this study, a mathematical model was developed to determine the possible cause of this outbreak. The most important parameters found to underlie the pattern of a small outbreak in 2013 and a much larger one in 2014 was the timing of the first imported and locally transmitted case. The importance of precipitation and temperature was also confirmed by the simulation results under different climate scenarios. The model also suggests that the earlier and more frequent control interventions in 2014 targeting immature mosquitoes, such as emptying water containers, and adult control, were effective in preventing larger outbreaks. Furthermore, more attention should be paid to imported cases occurring between March 1 st and July 1 st to prevent early and prolonged transmission. Without early detection and response, the final outbreak size might otherwise be an order of magnitude or more the size when the imported case occurred outside this time period.

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          Most cited references 34

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          Critical review of the vector status of Aedes albopictus.

           N G Gratz (2004)
          The mosquito Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae), originally indigenous to South-east Asia, islands of the Western Pacific and Indian Ocean, has spread during recent decades to Africa, the mid-east, Europe and the Americas (north and south) after extending its range eastwards across Pacific islands during the early 20th century. The majority of introductions are apparently due to transportation of dormant eggs in tyres. Among public health authorities in the newly infested countries and those threatened with the introduction, there has been much concern that Ae. albopictus would lead to serious outbreaks of arbovirus diseases (Ae. albopictus is a competent vector for at least 22 arboviruses), notably dengue (all four serotypes) more commonly transmitted by Aedes (Stegomyia) aegypti (L.). Results of many laboratory studies have shown that many arboviruses are readily transmitted by Ae. albopictus to laboratory animals and birds, and have frequently been isolated from wild-caught mosquitoes of this species, particularly in the Americas. As Ae. albopictus continues to spread, displacing Ae. aegypti in some areas, and is anthropophilic throughout its range, it is important to review the literature and attempt to predict whether the medical risks are as great as have been expressed in scientific journals and the popular press. Examination of the extensive literature indicates that Ae. albopictus probably serves as a maintenance vector of dengue in rural areas of dengue-endemic countries of South-east Asia and Pacific islands. Also Ae. albopictus transmits dog heartworm Dirofilaria immitis (Leidy) (Spirurida: Onchocercidae) in South-east Asia, south-eastern U.S.A. and both D. immitis and Dirofilaria repens (Raillet & Henry) in Italy. Despite the frequent isolation of dengue viruses from wild-caught mosquitoes, there is no evidence that Ae. albopictus is an important urban vector of dengue, except in a limited number of countries where Ae. aegypti is absent, i.e. parts of China, the Seychelles, historically in Japan and most recently in Hawaii. Further research is needed on the dynamics of the interaction between Ae. albopictus and other Stegomyia species. Surveillance must also be maintained on the vectorial role of Ae. albopictus in countries endemic for dengue and other arboviruses (e.g. Chikungunya, EEE, Ross River, WNV, LaCrosse and other California group viruses), for which it would be competent and ecologically suited to serve as a bridge vector.
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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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              Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever.

              Serum specimens collected during a prospective study of dengue infections among schoolchildren in Bangkok were tested for their ability to enhance dengue 2 (DEN-2) virus growth in human monocytes in vitro. Two groups of dengue-immune sera were compared: 32 dengue antibody positive serum specimens from children who subsequently developed asymptomatic secondary dengue infections; and 9 dengue antibody positive serum specimens from children who subsequently developed severe symptomatic secondary dengue infections, 8 of which were clinically diagnosed as dengue hemorrhagic fever. Antibody-dependent enhancement of virus growth was quantitated by measurement of virus yields in supernatant fluids of normal human monocyte cultures that were infected with DEN-2 virus in the presence of undiluted test serum. Only 4 of 32 (12%) preinfection sera from asymptomatic children, but 6 of 9 (67%) preinfection sera from symptomatic children, had significant enhancing activity (P less than 0.001). High serum DEN-2 antibody dependent enhancing activity is a significant (relative risk = 6.2) risk factor for severe illness among children in a dengue hemorrhagic fever endemic region. Dengue antibodies can be neutralizing and therefore protective, or they can be enhancing and increase the risk of dengue hemorrhagic fever.
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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
                10 February 2016
                February 2016
                : 10
                : 2
                Affiliations
                [1 ]Ministry of Education Key Laboratory for Earth System Modeling, Center for Earth System Science, Tsinghua University, Beijing, People’s Republic of China
                [2 ]Environmental Health Sciences, School of Public Health, University of California, Berkeley, Berkeley, California, United States of America
                [3 ]Department of Infectious Diseases, Guangzhou Center for Disease Control and Prevention, Guangzhou, People’s Republic of China
                [4 ]Department of Medical Statistics and Epidemiology, School of Public Health, Sun Yat-Sen University, Guangzhou, People’s Republic of China
                [5 ]Divisions of Biostatistics and Epidemiology, School of Public Health, University of California, Berkeley, Berkeley, California, United States of America
                [6 ]Joint Center for Global Change Studies, Beijing, People’s Republic of China
                Santa Fe Institute, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: QC QJ RCS JMM ZY PG. Analyzed the data: QC QJ RCS JMM ZY PG. Contributed reagents/materials/analysis tools: QJ ZY. Wrote the paper: QC QJ RCS PG.

                Article
                PNTD-D-15-01756
                10.1371/journal.pntd.0004417
                4749339
                26863623
                © 2016 Cheng 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.

                Page count
                Figures: 7, Tables: 3, Pages: 22
                Product
                Funding
                QC received financial support from the China Scholarship Council. QJ is funded by Guangdong Natural Science Foundation (No. S2013010013637), the Collaborative innovation project of Bureau of Science and Technology of Guagnzhou Municipality (No. 201508020263), the Project of Key Medicine Discipline Construction of Guangzhou Municipality (No. 2013-2015-07), and the Bureau of Health of Guangzhou Municipality (No.20141A011057) for funding. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Custom metadata
                The number of daily reported new cases was obtained from the Health Department of Guangdong Province ( http://www.gdwst.gov.cn/). The monthly average mosquito surveillance data was provided in the supporting information file S1 Table. Daily temperature, rainfall and evaporation data were downloaded from the China Meteorological Data Sharing Service System (CMDSSS ( http://cdc.nmic.cn/). Population data was obtained from the Guangdong Statistical Yearbook on China Infobank ( http://www.bjinfobank.com/).

                Infectious disease & Microbiology

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