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      Incidence dynamics and investigation of key interventions in a dengue outbreak in Ningbo City, China

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          Abstract

          Background

          The reported incidence of dengue fever increased dramatically in recent years in China. This study aimed to investigate and to assess the effectiveness of intervention implemented in a dengue outbreak in Ningbo City, Zhejiang Province, China.

          Methods

          Data of a dengue outbreak were collected in Ningbo City in China by a field epidemiological survey according to a strict protocol and case definition. Serum specimens of all cases were collected for diagnosis and the virological characteristics were detected by using polymerase chain reaction (PCR) and gene sequencing. Vector surveillance was implemented during the outbreak to collect the larva and adult mosquito densities to calculate the Breteau Index (BI) and human biting rate (HBR), respectively. Data of monthly BI and light-trap density in 2018 were built to calculate the seasonality of the vector. A transmission mathematical model was developed to dynamic the incidence of the disease. The parameters of the model were estimated by the data of the outbreak and vector surveillance data in 2018. The effectiveness of the interventions implemented during the outbreak was assessed by the data and the modelling.

          Results

          From 11 August to 8 September, 2018, a dengue outbreak was reported with 27 confirmed cases in a population of 5536-people community (community A) of Ningbo City. Whole E gene sequences were obtained from 24 cases and were confirmed as dengue virus type 1 (DENV-1). The transmission source of the outbreak was origin from community B where a dengue case having the same E gene sequence was onset on 30 July. Aedes albopictus was the only vector species in the area. The value of BI and HBR was 57.5 and 12 per person per hour respectively on 18 August, 2018 and decreased dramatically after interventions. The transmission model fitted well ( χ 2 = 6.324, P = 0.388) with the reported cases data. With no intervention, the total simulated number of the cases would be 1728 with a total attack rate (TAR) of 31.21% (95%CI: 29.99%– 32.43%). Case isolation and larva control (LC) have almost the same TAR and duration of outbreak (DO) as no intervention. Different levels of reducing HBR (rHBR) had different effectiveness with TARs ranging from 1.05% to 31.21% and DOs ranging from 27 days to 102 days. Adult vector control (AVC) had a very low TAR and DO. “LC+AVC” had a similar TAR and DO as that of AVC. “rHBR 100%+LC”, “rHBR 100%+AVC”, “rHBR 100%+LC+AVC” and “rHBR 100%+LC+AVC+Iso” had the same effectiveness.

          Conclusions

          Without intervention, DENV-1 could be transmitted rapidly within a short period of time and leads to high attack rate in community in China. AVC or rHBR should be recommended as primary interventions to control rapid transmission of the dengue virus at the early stage of an outbreak.

          Author summary

          Dengue has led to heavy disease burden in China. The reported incidence of the disease increased dramatically in recent years and cases have expanded from southern to central and northern part of China. In this study, the findings include that DENV-1 can transmit rapidly with a short period of time and leads to high attack rate in community, and that rHBR or AVC should be recommended as primary interventions to control rapid transmission of dengue virus at the early stage of an outbreak. Therefore, dengue outbreak is at high risk in many areas in China because of the potential high receptivity (widely distribution of Ae. albopictus) and vulnerability (high frequency of the importation) of the transmission. The high transmissibility of the virus makes it hard and urgent to control the outbreak. Delayed intervention (larvae control or case isolation) is hard to show its effectiveness and the interventions without delay are strongly recommended. Bed net or mosquito repellents were encouraged to use in the community to reduce HBR, and space spraying of insecticides were recommended to control adult vector during the outbreak.

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          Most cited references19

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          Dengue Fever in mainland China.

          Dengue is an acute emerging infectious disease transmitted by Aedes mosquitoes and has become a serious global public health problem. In mainland China, a number of large dengue outbreaks with serious consequences have been reported as early as 1978. In the three decades from 1978 to 2008, a total of 655,324 cases were reported, resulting in 610 deaths. Since the 1990s, dengue epidemics have spread gradually from Guangdong, Hainan, and Guangxi provinces in the southern coastal regions to the relatively northern and western regions including Fujian, Zhejiang, and Yunnan provinces. As the major transmission vectors of dengue viruses, the biological behavior and vectorial capacity of Aedes mosquitoes have undergone significant changes in the last two decades in mainland China, most likely the result of urbanization and global climate changes. In this review, we summarize the geographic and temporal distributions, the serotype and genotype distributions of dengue viruses in mainland China, and analyze the current status of surveillance and control of vectors for dengue transmission.
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            The changing epidemiology of dengue in China, 1990-2014: a descriptive analysis of 25 years of nationwide surveillance data

            Background Dengue has been a notifiable disease in China since 1 September 1989. Cases have been reported each year during the past 25 years of dramatic socio-economic changes in China, and reached a historical high in 2014. This study describes the changing epidemiology of dengue in China during this period, to identify high-risk areas and seasons and to inform dengue prevention and control activities. Methods We describe the incidence and distribution of dengue in mainland China using notifiable surveillance data from 1990-2014, which includes classification of imported and indigenous cases from 2005-2014. Results From 1990-2014, 69,321 cases of dengue including 11 deaths were reported in mainland China, equating to 2.2 cases per one million residents. The highest number was recorded in 2014 (47,056 cases). The number of provinces affected has increased, from a median of three provinces per year (range: 1 to 5 provinces) during 1990-2000 to a median of 14.5 provinces per year (range: 5 to 26 provinces) during 2001-2014. During 2005-2014, imported cases were reported almost every month and 28 provinces (90.3%) were affected. However, 99.8% of indigenous cases occurred between July and November. The regions reporting indigenous cases have expanded from the coastal provinces of southern China and provinces adjacent to Southeast Asia to the central part of China. Dengue virus serotypes 1, 2, 3, and 4 were all detected from 2009-2014. Conclusions In China, the area affected by dengue has expanded since 2000 and the incidence has increased steadily since 2012, for both imported and indigenous dengue. Surveillance and control strategies should be adjusted to account for these changes, and further research should explore the drivers of these trends. Please see related article: http://dx.doi.org/10.1186/s12916-015-0345-0 Electronic supplementary material The online version of this article (doi:10.1186/s12916-015-0336-1) contains supplementary material, which is available to authorized users.
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              Dynamic Epidemiological Models for Dengue Transmission: A Systematic Review of Structural Approaches

              Dengue is a vector-borne disease recognized as the major arbovirose with four immunologically distant dengue serotypes coexisting in many endemic areas. Several mathematical models have been developed to understand the transmission dynamics of dengue, including the role of cross-reactive antibodies for the four different dengue serotypes. We aimed to review deterministic models of dengue transmission, in order to summarize the evolution of insights for, and provided by, such models, and to identify important characteristics for future model development. We identified relevant publications using PubMed and ISI Web of Knowledge, focusing on mathematical deterministic models of dengue transmission. Model assumptions were systematically extracted from each reviewed model structure, and were linked with their underlying epidemiological concepts. After defining common terms in vector-borne disease modelling, we generally categorised fourty-two published models of interest into single serotype and multiserotype models. The multi-serotype models assumed either vector-host or direct host-to-host transmission (ignoring the vector component). For each approach, we discussed the underlying structural and parameter assumptions, threshold behaviour and the projected impact of interventions. In view of the expected availability of dengue vaccines, modelling approaches will increasingly focus on the effectiveness and cost-effectiveness of vaccination options. For this purpose, the level of representation of the vector and host populations seems pivotal. Since vector-host transmission models would be required for projections of combined vaccination and vector control interventions, we advocate their use as most relevant to advice health policy in the future. The limited understanding of the factors which influence dengue transmission as well as limited data availability remain important concerns when applying dengue models to real-world decision problems.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: Resources
                Role: Data curationRole: Investigation
                Role: Formal analysis
                Role: MethodologyRole: Validation
                Role: Data curationRole: Investigation
                Role: Formal analysis
                Role: Writing – review & editing
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: Formal analysis
                Role: Formal analysis
                Role: Formal analysis
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: Resources
                Role: ConceptualizationRole: MethodologyRole: SoftwareRole: SupervisionRole: 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
                15 August 2019
                August 2019
                : 13
                : 8
                : e0007659
                Affiliations
                [1 ] Ningbo Municipal Center for Disease Control and Prevention, Ningbo City, Zhejiang Province, People’s Republic of China
                [2 ] State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, School of Public Health, Xiamen University, Xiamen City, Fujian Province, People’s Republic of China
                [3 ] School of Science, Beijing University of Civil Engineering and Architecture, Beijing, People's Republic of China
                [4 ] Haishu District Center for Disease Control and Prevention, Ningbo City, Zhejiang Province, People’s Republic of China
                [5 ] Center for Disease Control and Prevention, Health Bureau, Macao SAR, People’s Republic of China
                Institute for Disease Modeling, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-0710-5086
                Article
                PNTD-D-18-02042
                10.1371/journal.pntd.0007659
                6711548
                31415559
                3ad91431-73b3-4cd8-b503-cb9ee5947f4b
                © 2019 Yi 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
                : 5 January 2019
                : 24 July 2019
                Page count
                Figures: 7, Tables: 3, Pages: 23
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100011438, State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics;
                Award ID: SKLVD2018KF001
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100011438, State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics;
                Award ID: SKLVD2018KF002
                Award Recipient :
                Funded by: Zhejiang Medical Key Discipline
                Award ID: 07–013
                Award Recipient :
                Funded by: Ningbo Health Branding Subject Fund
                Award ID: PPXK2018-10
                Award Recipient :
                Funded by: Zhejiang Medicine Health Science and Technology Project
                Award ID: 2019KY634
                Award Recipient :
                This study was partly supported by the Open Research Fund of State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics (SKLVD2018KF001 and SKLVD2018KF002), the Zhejiang Medical Key Discipline (07–013), the Ningbo Health Branding Subject Fund (PPXK2018-10), and the Zhejiang Medicine Health Science and Technology Project (2019KY634). 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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                Research and Analysis Methods
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                2019-08-27
                All relevant data are within the manuscript and its Supporting Information files.

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