Phylodynamics unveils invading and diffusing patterns of dengue virus serotype-1 in Guangdong, China from 1990 to 2019 under a global genotyping framework

Zhao，Lingzhai1; Guo，Xiang2; Li，Liqiang3; Jing，Qinlong4; Ma，Jinmin5; Xie，Tian2; Lin，Dechun5; Li，Li6; Yin，Qingqing2; Wang，Yuji2; Zhang，Xiaoqing2; Li，Ziyao2; Liu，Xiaohua2; Hu，Tian2; Hu，Minling2; Ren，Wenwen2; Li，Jun7; Peng，Jie8; Yu，Lei1; Peng，Zhiqiang9; Hong，Wenxin1; Leng，Xingyu1; Luo，Lei4; Ngobeh，Jone Jama Kpanda2; Tang，Xiaoping1; Wu，Rangke10; Zhao，Wei11; Shi，Benyun12; Liu，Jiming13; Yang，Zhicong4; Chen，Xiao Guang2; Zhou，Xiaohong2; Zhang，Fuchun1,14

2024-12-01

10.1186/s40249-024-01211-6

Infectious Diseases of Poverty   影响因子和分区

2095-5162

2049-9957

Background: The strong invasiveness and rapid expansion of dengue virus (DENV) pose a great challenge to global public health. However, dengue epidemic patterns and mechanisms at a genetic scale, particularly in term of cross-border transmissions, remain poorly understood. Importation is considered as the primary driver of dengue outbreaks in China, and since 1990 a frequent occurrence of large outbreaks has been triggered by the imported cases and subsequently spread to the western and northern parts of China. Therefore, this study aims to systematically reveal the invasion and diffusion patterns of DENV-1 in Guangdong, China from 1990 to 2019. Methods: These analyses were performed on 179 newly assembled genomes from indigenous dengue cases in Guangdong, China and 5152 E gene complete sequences recorded in Chinese mainland. The genetic population structure and epidemic patterns of DENV-1 circulating in Chinese mainland were characterized by phylogenetics, phylogeography, phylodynamics based on DENV-1 E-gene-based globally unified genotyping framework. Results: Multiple serotypes of DENV were co-circulating in Chinese mainland, particularly in Guangdong and Yunnan provinces. A total of 189 transmission clusters in 38 clades belonging to 22 subgenotypes of genotype I, IV and V of DENV-1 were identified, with 7 Clades of Concern (COCs) responsible for the large outbreaks since 1990. The epidemic periodicity was inferred from the data to be approximately 3 years. Dengue transmission events mainly occurred from Great Mekong Subregion-China (GMS-China), Southeast Asia (SEA), South Asia Subcontinent (SASC), and Oceania (OCE) to coastal and land border cities respectively in southeastern and southwestern China. Specially, Guangzhou was found to be the most dominant receipting hub, where DENV-1 diffused to other cities within the province and even other parts of the country. Genome phylogeny combined with epidemiological investigation demonstrated a clear local consecutive transmission process of a 5C1 transmission cluster (5C1-CN4) of DENV-1 in Guangzhou from 2013 to 2015, while the two provinces of Guangdong and Yunnan played key roles in ongoing transition of dengue epidemic patterns. In contextualizing within Invasion Biology theories, we have proposed a derived three-stage model encompassing the stages of invasion, colonization, and dissemination, which is supposed to enhance our understanding of dengue spreading patterns. Conclusions: This study demonstrates the invasion and diffusion process of DENV-1 in Chinese mainland within a global genotyping framework, characterizing the genetic diversities of viral populations, multiple sources of importation, and periodic dynamics of the epidemic. These findings highlight the potential ongoing transition trends from epidemic to endemic status offering a valuable insight into early warning, prevention and control of rapid spreading of dengue both in China and worldwide. Graphical Abstract: (Figure presented.)

China Dengue serotype-1 Epidemic periodicity Genetic population structure Global genotyping framework Molecular epidemiology Phylodynamics Phylogeography

SCI

英语

其他

2-s2.0-85195888300

Scopus

1.Institute of Infectious Diseases,Guangzhou Eighth People’s Hospital,Guangzhou Medical University,Guangzhou,Guangdong,510440,China
2.Department of Pathogen Biology,School of Public Health,Institute of Tropical Medicine,Southern Medical University; Guangdong Provincial Key Laboratory of Tropical Disease Research; Key Laboratory of Prevention and Control for Emerging Infectious Diseases of Guangdong Higher Institutes; Key Laboratory of Infectious Diseases Research in South China of Ministry of Education,Guangzhou,510515,China
3.Department of Clinical Laboratory,The Third People’s Hospital of Shenzhen,Southern University of Science and Technology,National Clinical Research Center for Infectious Diseases,Guangdong Provincial Clinical Research Center for Infectious Diseases (Tuberculosis),Shenzhen Clinical Research Center for Tuberculosis,Shenzhen,China
4.Guangzhou Center for Disease Control and Prevention,Guangzhou,510440,China
5.BGI-Shenzhen,Shenzhen,518083,China
6.Department of Biostatistics,School of Public Health,State Key Laboratory of Organ Failure Research,Guangdong Provincial Key Laboratory of Tropical Disease Research,Southern Medical University,Guangzhou,510515,China
7.Guangdong Provincial Key Laboratory of Research On Emergency in TCM,Guangdong Provincial Hospital of Traditional Chinese Medicine,Guangzhou,510120,China
8.Department of Infectious Diseases,Nanfang Hospital,Southern Medical University,Guangzhou,510515,China
9.Guangdong Provincial Center for Disease Control and Prevention,Guangzhou,511430,China
10.The School of Foreign Studies,Southern Medical University,Guangzhou,510515,China
11.BSL-3 Laboratory(Guangdong),School of Public Health,Southern Medical University,Guangzhou,510515,China
12.College of Computer and Information Engineering,Nanjing Tech University,Nanjing,211816,China
13.Department of Computer Science,Hong Kong Baptist University,999077,Hong Kong
14.Guangzhou Medical Research Institute of Infectious Diseases,Infectious Disease Center,Guangzhou Eighth People’s Hospital,Guangzhou Medical University,Guangzhou,510440,China

Zhao，Lingzhai,Guo，Xiang,Li，Liqiang,et al. Phylodynamics unveils invading and diffusing patterns of dengue virus serotype-1 in Guangdong, China from 1990 to 2019 under a global genotyping framework[J]. Infectious Diseases of Poverty,2024,13(1).

Zhao，Lingzhai.,Guo，Xiang.,Li，Liqiang.,Jing，Qinlong.,Ma，Jinmin.,...&Zhang，Fuchun.(2024).Phylodynamics unveils invading and diffusing patterns of dengue virus serotype-1 in Guangdong, China from 1990 to 2019 under a global genotyping framework.Infectious Diseases of Poverty,13(1).

Zhao，Lingzhai,et al."Phylodynamics unveils invading and diffusing patterns of dengue virus serotype-1 in Guangdong, China from 1990 to 2019 under a global genotyping framework".Infectious Diseases of Poverty 13.1(2024).