TY - JOUR
T1 - Phylodynamics unveils invading and diffusing patterns of dengue virus serotype-1 in Guangdong, China from 1990 to 2019 under a global genotyping framework
AU - Zhao, Lingzhai
AU - Guo, Xiang
AU - Li, Liqiang
AU - Jing, Qinlong
AU - Ma, Jinmin
AU - Xie, Tian
AU - Lin, Dechun
AU - Li, Li
AU - Yin, Qingqing
AU - Wang, Yuji
AU - Zhang, Xiaoqing
AU - Li, Ziyao
AU - Liu, Xiaohua
AU - Hu, Tian
AU - Hu, Minling
AU - Ren, Wenwen
AU - Li, Jun
AU - Peng, Jie
AU - Yu, Lei
AU - Peng, Zhiqiang
AU - Hong, Wenxin
AU - Leng, Xingyu
AU - Luo, Lei
AU - Ngobeh, Jone Jama Kpanda
AU - Tang, Xiaoping
AU - Wu, Rangke
AU - Zhao, Wei
AU - Shi, Benyun
AU - Liu, Jiming
AU - Yang, Zhicong
AU - Chen, Xiao Guang
AU - Zhou, Xiaohong
AU - Zhang, Fuchun
N1 - Publisher Copyright:
© The Author(s) 2024.
Funding information:
This study was supported by the National Key R&D Program of China (2020YFC1200100 and 2016YFC1200500), the Guangzhou Synergy Innovation Key for Health (201803040006 and 201508020263), Key R&D Program of Guangdong Province (2022B1111030002), the National Institutes of Health, USA (AI136850), the National Natural Science Foundation of China (82072311), the Guangzhou International Science and Technology Cooperation Program (2012J5100026), the Basic and Applied Basic Research Projects were jointly funded by the University of Guangzhou (2023A03J0810), the Guangdong Science and Technology Program Key Projects (2021A1515220017), the Guangzhou Health Science and Technology Project (2021A031004), and the General Guidance Project of Guangzhou Municipal Health Commission (20211A010048).
PY - 2024/6/11
Y1 - 2024/6/11
N2 - 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.
AB - 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.
KW - China
KW - Dengue serotype-1
KW - Epidemic periodicity
KW - Genetic population structure
KW - Global genotyping framework
KW - Molecular epidemiology
KW - Phylodynamics
KW - Phylogeography
UR - http://www.scopus.com/inward/record.url?scp=85195888300&partnerID=8YFLogxK
UR - https://idpjournal.biomedcentral.com/articles/10.1186/s40249-024-01211-6
U2 - 10.1186/s40249-024-01211-6
DO - 10.1186/s40249-024-01211-6
M3 - Journal article
C2 - 38863070
AN - SCOPUS:85195888300
SN - 2095-5162
VL - 13
JO - Infectious Diseases of Poverty
JF - Infectious Diseases of Poverty
M1 - 43
ER -
