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The Origin and Molecular Epidemiology of Dengue Fever in Hainan Province, China, 2019

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The Origin and Molecular Epidemiology of Dengue Fever in Hainan Province, China, 2019 fmicb-12-657966 March 23, 2021 Time: 13:14 # 1 ORIGINAL RESEARCH published: 24 March 2021 doi: 10.3389/fmicb.2021.657966 The Origin and Molecular Epidemiology of Dengue Fever in Hainan Province, China, 2019 Lin Liu1†, Tao Wu2†, Biao Liu1, Rajaofera Mamy Jayne Nelly1, Yumei Fu1, Xun Kang1, Chuizhe Chen1, Zenyan Huang1, Biao Wu2, Jiao Wang2, Zhongyi Zhu3,4, Jinmin Ma3, Ming Liu2, Yanru Zhang2, Chuanyu Bao5, Feng Lin2*, Weijun Chen3,4* and Qianfeng Xia1* 1 NHC Key Laboratory of Control of Tropical Diseases, Key Laboratory of Tropical Translational Medicine of Ministry of Education, School of Tropical Medicine and Laboratory Medicine, Hainan Medical University, Haikou, China, 2 Department of Infectious Diseases, Hainan General Hospital, Hainan Affiliated Hospital of Hainan Medical University, Haikou, China, 3 BGI PathoGenesis Pharmaceutical Technology, BGI-Shenzhen, Shenzhen, China, 4 BGI Education Center, University of Chinese Academy of Sciences, Shenzhen, China, 5 Department of Emergency Surgery, Hainan General Hospital, Hainan Affiliated Hospital of Hainan Medical University, Haikou, China Edited by: There was an outbreak of Dengue fever on September 5, 2019, in Hainan Province, Chunfu Zheng, Fujian Medical University, China which has not been endemic for 28 years. We aim to describe the clinical and Reviewed by: epidemiological features of the 2019 outbreak in Hainan Province and identify the cause. Gong Cheng, All type 1 Dengue fever cases that occurred in this outbreak of Hainan exhibited mild Tsinghua University, China Xiaoming Wang, clinical symptoms. The epidemiological investigations indicate that the outbreak might University of California, Irvine, originate from workers in the Xiuying area, Haikou City, form a concentrated outbreak, United States and then spread out. Bayesian phylogenies results and epidemiological data were used *Correspondence: to infer a likely series of events for the dengue virus’s potential spread and trace the Feng Lin [email protected] possible sources. The strains’ sequences were close to a sequence from the nearby Weijun Chen Guangdong province, supporting the hypothesis that the dengue virus was imported [email protected] Qianfeng Xia from Guangdong province and then spread across Hainan province. Furthermore, it [email protected] is interesting that two other strains didn’t group with this cluster, suggesting that †These authors have contributed additional introduction pathways might exist. The study indicated that the dengue fever equally to this work epidemic presented two important modes in Hainan. Firstly, epidemics prevalence was Specialty section: caused by imported cases, and then endogenous epidemics broke out in the natural This article was submitted to epidemic focus. Virology, a section of the journal Keywords: dengue fever, molecular-characteristics, bayesian phylogenies, hainan province, epidemiological Frontiers in Microbiology Received: 24 January 2021 Accepted: 02 March 2021 INTRODUCTION Published: 24 March 2021 Citation: Dengue fever (DF), a mosquito-borne viral infection common in warm, tropical climates,is an Liu L, Wu T, Liu B, Nelly RMJ, acute infectious disease caused by the Dengue virus (DENV). Since the first reported outbreak Fu Y, Kang X, Chen C, Huang Z, in 1779 in Jakarta, Indonesia, outbreaks have frequently been found in tropical and sub-tropical Wu B, Wang J, Zhu Z, Ma J, Liu M, climates worldwide, mostly in urban and semi-urban areas with local variations in risk influenced Zhang Y, Bao C, Lin F, Chen W and by rainfall, temperature, and relative humidity (Guzman et al., 2013; Halstead and Cohen, 2015; Xia Q (2021) The Origin and Molecular Epidemiology of Dengue Fever Niyati and Ira, 2016). The incidence of dengue has grown dramatically around the world in recent in Hainan Province, China, 2019. decades. One study on dengue prevalence estimates that 3.9 billion people are at risk of dengue Front. Microbiol. 12:657966. viruses (Brady et al., 2012; Bhatt et al., 2013). Despite a risk of infection in 128 countries, 70% of the doi: 10.3389/fmicb.2021.657966 actual burden is in Asia. Frontiers in Microbiology| www.frontiersin.org 1 March 2021| Volume 12| Article 657966 fmicb-12-657966 March 23, 2021 Time: 13:14 # 2 Liu et al. Molecular Epidemiology of Dengue Fever The first recorded outbreak of DF in China occurred in based on the epidemiological history, clinical manifestations, Guangdong province in 1978. It was caused by DENV-3 imported and laboratory examination. The serum samples from confirmed from countries in south-east Asia. Since then, imported dengue cases at the different infection times and different areas (from fever cases have often caused local outbreaks in provinces like Haikou, Danzhou, Wanning, Lingshui, Wencang cities) were Guangxi, Yunnan, Hainan, Fujian, etc., in China (Wang et al., collected for dengue virus gene sequencing and E gene analysis. 2018; Zhang et al., 2019). Two large outbreaks of dengue virus In this epidemiological report, we used data from September 5, type 1 and dengue virus type 3 were recorded, respectively, during 2019 to October 17, 2019, to describe the disease’s clinical and 2006–2007 and 2012–2015 (Sang et al., 2014; Zhang et al., 2019). epidemiological features and explore where the DENV virus in Hainan is the southernmost province and the second largest Hainan originally came from and what shaped their evolution. island in China, with Guangdong province across the Qiongzhou Strait to the north. It is a tropical monsoon climate with a rainy Laboratory Diagnostic Assays season from May to October. The meteorological conditions A total of 6 serum samples were selected for whole-genome are favorable for the breeding of Aedes mosquito larvae and sequencing, and 90 DENV-positive sera were collected the transmission of DF. There were three DF epidemics in the to amplify and sequence the E gene by The Beijing epidemiological history of Hainan. The first one was caused Genomics Institute (BGI). Sequence-dependent single primer by dengue virus type 3 in 1978 (Fan et al., 1989). Then there amplification(SDSPA)was used to enrich the viral nucleic acid, was a second struck in 1985–1988, and a third one, a dengue construct the sequencing library, and PE150 strategy was selected hemorrhagic fever in 1991, both caused by dengue virus type 2 for sequencing on the MGI-2000 sequencing instrument (BGI, (Qiu et al., 1991). Ever since 1991, there were no more outbreaks. CHN). Nucleic acids were extracted using QIAamp Viral RNA In August 2019, several workers in the Wuyuan River area Mini Kit (52904#, QIAGEN). of Xiuying District, Haikou City, experienced fever, fatigue, and rashes. After further testing for NS1 antigen and dengue virus Phylogenetic Analysis nucleic acid, the first case of dengue fever was diagnosed in Multiple sequence alignment was done by MUSCLE (V3.8.31) Hainan General Hospital on September 5, 2019. Subsequently, with a maximum number of iterations of 16. The maximum close contacts of confirmed cases and those with suspicious likelihood (ML) phylogenetic trees were estimated by FastTree exposures to the Wuyuan River area were screened, and a (Version: 2.1) of multiple alignment sequences, with nucleotide follow-up study by health professionals found multiple suspicious distances calculated using the Jukes-Cantor nucleotide fever cases around the epidemic site. The Hainan Centre substitution model and branch lengths inferred by CAT for Disease Control conducted epidemiological investigations, approximation with 20 rate categories. Final ML trees (both sampling inspections, and mosquito control treatments on the the topology and the branch lengths) were improved by epidemic site. After further testing for NS1 antigen and dengue Normal C NNI C SPR (2 rounds range 10) C ML-NNI opt-each virus nucleic acid, multiple DF cases were diagnosed, and the heuristic tree search algorithms. Local support values with local outbreak of dengue fever was confirmed. Altogether 5 1,000 replicates calculated by the Shimodaira-Hasegawa test cities and towns throughout the province reported the local (SH-like local supports) were estimated to assess each split’s epidemic situation (Haikou, Wenchang, Danzhou, Lingshui, and robustness in the tree. Wanning). A total of 264 confirmed dengue cases were reported in Hainan Province from September 5, 2019 to October 17, 2019. Molecular Dating Using BEAST In this study, we described the clinical and epidemiological Bayesian phylogenies were performed in BEASTv.2.6.0 features of the 2019 dengue fever outbreak and determined the (Bouckaert et al., 2019). The substitution model was estimated by complete genome sequences of 6 dengue isolates collected and E the J model test (V2.1.10) to access the most suitable nucleotide gene sequences from 90 patients in Hainan during the epidemic. model with the default parameter to access 88 potential-based In combination with those published sequences in GenBank, we substitution models. The GTR C G model is selected based on conducted an extensive molecular epidemiological analysis to best fit Bayesian information criterion (BIC) score evaluated determine where the DENV isolates in Hainan originally came by J model test. A strike clock rate combined with Coalescent from and what shaped their evolution, which is important to Constant Population model was used to evaluate the most dengue control and prevention. recent common ancestor (MRCA) prior to each clade (Russel et al., 2019). Finally, Tree Annotator v2.5.2 was applied to MATERIALS AND METHODS summarize Maximum-clade credibility trees of all MCMC trees with posterior probability values reported in each node. Collection of Isolates and Clinical Information RESULTS According to the Chinese Center for Disease Control and Prevention in 2018 issued by the Dengue Fever Prevention and Epidemiology Control of Technical Guidelines and Criteria for the diagnosis Between September 5, 2019 and October 17, 2019, 3941 suspected of dengue (WS216 2018), an outbreak of dengue fever was cases were identified, 264 cases were confirmed dengue fever definition in Hainan. The dengue diagnosis was confirmed with PCR positive and NS1 antigen positive in hospital.
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