The epidemiology and evolutionary dynamics of massive dengue outbreak in China, 2019

Introduction In 2019, China experienced massive dengue outbreaks with high incidence and expanded outbreak areas. The study aims to depict dengue’s epidemiology and evolutionary dynamics in China and explore the possible origin of these outbreaks. Methods Records of confirmed dengue cases in 2019 were obtained from the China Notifiable Disease Surveillance System. The sequences of complete envelope gene detected from the outbreak provinces in China in 2019 were retrieved from GenBank. Maximum Likelihood trees were constructed to genotype the viruses. The median-joining network was used to visualize fine-scale genetic relationships. Four methods were used to estimate the selective pressure. Results A total of 22,688 dengue cases were reported, 71.4% of which were indigenous cases and 28.6% were imported cases (including from abroad and from other domestic provinces). The abroad cases were predominantly imported from Southeast Asia countries (94.6%), with Cambodia (3,234 cases, 58.9%), and Myanmar (1,097 cases, 20.0%) ranked as the top two. A total of 11 provinces with dengue outbreaks were identified in the central-south of China, of which Yunnan and Guangdong provinces had the highest number of imported and indigenous cases. The primary source of imported cases in Yunnan was from Myanmar, while in the other ten provinces, the majority of imported cases were from Cambodia. Guangdong, Yunnan and Guangxi provinces were China’s primary sources of domestically imported cases. Phylogenetic analysis of the viruses in outbreak provinces revealed three genotypes: (I, IV, and V) in DENV 1, Cosmopolitan and Asian I genotypes in DENV 2, and two genotypes (I and III) in DENV 3. Some genotypes concurrently circulated in different outbreak provinces. Most of the viruses were clustered with those from Southeast Asia. Haplotype network analysis showed that Southeast Asia, possibly Cambodia and Thailand, was the respective origin of the viruses in clade 1 and 4 for DENV 1. Positive selection was detected at codon 386 in clade 1. Conclusion Dengue importation from abroad, especially from Southeast Asia, resulted in the dengue epidemic in China in 2019. Domestic transmission between provinces and positive selection on virus evolution may contribute to the massive dengue outbreaks.

[1]  W. Yin,et al.  Dengue Fever in Mainland China, 2005–2020: A Descriptive Analysis of Dengue Cases and Aedes Data , 2022, International journal of environmental research and public health.

[2]  D. Fontenille,et al.  Monitoring insecticide resistance of adult and larval Aedes aegypti (Diptera: Culicidae) in Phnom Penh, Cambodia , 2022, Parasites & vectors.

[3]  Qiyong Liu,et al.  The epidemiological characteristics of dengue in high-risk areas of China, 2013–2016 , 2021, PLoS neglected tropical diseases.

[4]  J. Pang,et al.  Global dengue importation: a systematic review , 2021, BMC Infectious Diseases.

[5]  Tao Liu,et al.  Co-benefits of nonpharmaceutical intervention against COVID-19 on infectious diseases in China: A large population-based observational study , 2021, The Lancet Regional Health - Western Pacific.

[6]  M. Quam,et al.  Global burden for dengue and the evolving pattern in the past 30 years. , 2021, Journal of travel medicine.

[7]  Zhongdao Wu,et al.  Dengue fever and dengue virus in the People's Republic of China , 2021, Reviews in medical virology.

[8]  Yuan Liu,et al.  Decreased dengue cases attributable to the effect of COVID-19 in Guangzhou in 2020 , 2021, PLoS neglected tropical diseases.

[9]  C. Sindato,et al.  Circulation of dengue serotype 1 viruses during the 2019 outbreak in Dar es Salaam, Tanzania , 2021, Pathogens and global health.

[10]  Guangchuang Yu,et al.  ggtreeExtra: Compact Visualization of Richly Annotated Phylogenetic Data , 2021, Molecular biology and evolution.

[11]  Y. Huang,et al.  Phylogenetic Analysis of the Dengue Virus Strains Causing the 2019 Dengue Fever Outbreak in Hainan, China , 2021, Virologica Sinica.

[12]  Jiang-feng Du,et al.  Phylogenetic Analysis of the Dengue Virus Strains Causing the 2019 Dengue Fever Outbreak in Hainan, China , 2021, Virologica Sinica.

[13]  A. Clements,et al.  Epidemiological Analysis of the 2019 Dengue Epidemic in Bhutan , 2021, International journal of environmental research and public health.

[14]  Xiaobo Liu,et al.  Comparative analyses on epidemiological characteristics of dengue fever in Guangdong and Yunnan, China, 2004–2018 , 2019, BMC Public Health.

[15]  R. Poudel,et al.  Molecular study of 2019 dengue fever outbreaks in Nepal. , 2020, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[16]  M. Ma,et al.  Imported Dengue Serotype 1 Outbreak in a Non-endemic Region, China, 2017: A Molecular and Seroepidemiological Study. , 2020, The Journal of infection.

[17]  Li-na Sun,et al.  Genomic epidemiological characteristics of dengue fever in Guangdong province, China from 2013 to 2017 , 2020, PLoS neglected tropical diseases.

[18]  S. Cauchemez,et al.  Predicting Dengue Outbreaks in Cambodia , 2019, Emerging infectious diseases.

[19]  A. Rodríguez-Morales,et al.  Dengue in Honduras and the Americas: The epidemics are back! , 2019, Travel medicine and infectious disease.

[20]  A. Samy,et al.  Mapping the global potential distributions of two arboviral vectors Aedes aegypti and Ae. albopictus under changing climate , 2018, PloS one.

[21]  Eduardo Massad,et al.  Estimating the probability of dengue virus introduction and secondary autochthonous cases in Europe , 2018, Scientific Reports.

[22]  Mutsuo Kobayashi,et al.  Dengue Virus Infection in Aedes albopictus during the 2014 Autochthonous Dengue Outbreak in Tokyo Metropolis, Japan. , 2018, The American journal of tropical medicine and hygiene.

[23]  Juan C. Sánchez-DelBarrio,et al.  DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. , 2017, Molecular biology and evolution.

[24]  K. Ebi,et al.  Dengue in a changing climate. , 2016, Environmental research.

[25]  D. Roiz,et al.  Autochthonous dengue outbreak in Nîmes, South of France, July to September 2015. , 2016, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[26]  David Bryant,et al.  popart: full‐feature software for haplotype network construction , 2015 .

[27]  Xiaobo Liu,et al.  Dengue is still an imported disease in China: a case study in Guangzhou. , 2015, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[28]  Jun Yang,et al.  Predicting Unprecedented Dengue Outbreak Using Imported Cases and Climatic Factors in Guangzhou, 2014 , 2015, PLoS neglected tropical diseases.

[29]  Eva Harris,et al.  Dengue , 2015, The Lancet.

[30]  Bian-Li Xu,et al.  Outbreak of dengue Fever in central China, 2013. , 2014, Biomedical and environmental sciences : BES.

[31]  Jian Wang,et al.  Severe dengue outbreak in Yunnan, China, 2013. , 2014, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[32]  K Khan,et al.  The 2012 dengue outbreak in Madeira: exploring the origins. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[33]  Sergei L. Kosakovsky Pond,et al.  FUBAR: a fast, unconstrained bayesian approximation for inferring selection. , 2013, Molecular biology and evolution.

[34]  E. Undurraga,et al.  Economic and Disease Burden of Dengue in Southeast Asia , 2013, PLoS neglected tropical diseases.

[35]  Sergei L. Kosakovsky Pond,et al.  Detecting Individual Sites Subject to Episodic Diversifying Selection , 2012, PLoS genetics.

[36]  Gail M. Williams,et al.  Spatiotemporal analysis of indigenous and imported dengue fever cases in Guangdong province, China , 2012, BMC Infectious Diseases.

[37]  Rubing Chen,et al.  Dengue — Quo tu et quo vadis? , 2011, Viruses.

[38]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[39]  Kazutaka Katoh,et al.  Multiple alignment of DNA sequences with MAFFT. , 2009, Methods in molecular biology.

[40]  Sergei L. Kosakovsky Pond,et al.  Not so different after all: a comparison of methods for detecting amino acid sites under selection. , 2005, Molecular biology and evolution.

[41]  P. Effler,et al.  Dengue Risk among Visitors to Hawaii during an Outbreak , 2005, Emerging infectious diseases.

[42]  Y. Modis,et al.  Variable Surface Epitopes in the Crystal Structure of Dengue Virus Type 3 Envelope Glycoprotein , 2005, Journal of Virology.

[43]  Y. Modis,et al.  Structure of the dengue virus envelope protein after membrane fusion , 2004, Nature.

[44]  Suh-Chin Wu,et al.  Structural Basis of a Flavivirus Recognized by Its Neutralizing Antibody , 2003, Journal of Biological Chemistry.

[45]  Wei Zhang,et al.  Structure of Dengue Virus Implications for Flavivirus Organization, Maturation, and Fusion , 2002, Cell.

[46]  H. Bandelt,et al.  Median-joining networks for inferring intraspecific phylogenies. , 1999, Molecular biology and evolution.