The dengue virus (DENV) is a vital global public health issue. The 2014 dengue epidemic in Guangzhou, China, caused approximately 40,000 cases of infection and five deaths. We carried out a comprehensive investigation aimed at identifying the transmission sources in this dengue epidemic. To analyze the phylogenetics of the 2014 dengue strains, the envelope (E) gene sequences from 17 viral strains isolated from 168 dengue patient serum samples were sequenced and a phylogenetic tree was reconstructed. All 17 strains were serotype I strains, including 8 genotype I and 9 genotype V strains. Additionally, 6 genotype I strains that were probably introduced to China from Thailand before 2009 were widely transmitted in the 2013 and 2014 epidemics, and they continued to circulate until 2015, with one affinis strain being found in Singapore. The other 2 genotype I strains were introduced from the Malaya Peninsula in 2014. The transmission source of the 9 genotype V strains was from Malaysia in 2014. DENVs of different serotypes and genotypes co-circulated in the 2014 dengue outbreak in Guangzhou. Moreover, not only had DENV been imported to Guangzhou, but it had also been gradually exported, as the viruses exhibited an enzootic transmission cycle in Guangzhou.
This work was supported by the Guangdong Natural Science Foundation (No. S2012030006598), the Science & Technology Planning Project of Guangdong Province of China (No. 2013A020229007), and the Innovative Program of the State Key Laboratory of Virology (No. 2016KF001). We would like to thank the China Center for Type Culture Collection for donating the C6/36 cells, and Jing Peng and Weiyong Liu from the Department of Clinical Laboratory, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, for their guidance on the phylogenetic analyses.
References
Andrade EH, Figueiredo LB, Vilela AP, Rosa JC, Oliveira JG, Zibaoui HM, Araujo VE, Miranda DP, Ferreira PC, Abrahao JS, Kroon EG. 2016. Spatial-temporal co-circulation of dengue virus 1, 2, 3, and 4 associated with coinfection cases in a hyperendemic area of Brazil: a 4-Week Survey. Am J Trop Med Hyg, 94: 1080–1084.CrossRefPubMedGoogle Scholar
Barreiro P. 2016. Evolving RNA virus pandemics: HIV, HCV, Ebola, Dengue, Chikunguya, and now Zika!. AIDS Rev, 18: 54–55.PubMedGoogle Scholar
Cheng Q, Jing Q, Spear RC, Marshall JM, Yang Z, Gong P. 2016. Climate and the timing of imported cases as determinants of the dengue outbreak in Guangzhou, 2014: evidence from a mathematical model. PLoS Negl Trop Dis, 10: e0004417.CrossRefPubMedPubMedCentralGoogle Scholar
Costa RL, Voloch CM, Schrago CG. 2012. Comparative evolutionary epidemiology of dengue virus serotypes. Infect Genet Evol, 12: 309–314.CrossRefPubMedGoogle Scholar
Cruz CD, Forshey BM, Juarez DS, Guevara C, Leguia M, Kochel TJ, Halsey ES. 2013. Molecular epidemiology of American/Asian genotype DENV-2 in Peru. Infect Genet Evol, 18: 220–228.CrossRefPubMedGoogle Scholar
Ditsuwan T, Liabsuetrakul T, Chongsuvivatwong V, Thammapalo S, McNeil E. 2011. Assessing the spreading patterns of dengue infection and chikungunya fever outbreaks in lower southern Thailand using a geographic information system. Ann Epidemiol, 21: 253–261.CrossRefPubMedGoogle Scholar
Drumond BP, Mondini A, Schmidt DJ, Bosch I, Nogueira ML. 2012. Population dynamics of DENV-1 genotype V in Brazil is characterized by co-circulation and strain/lineage replacement. Arch Virol, 157: 2061–2073.CrossRefPubMedGoogle Scholar
Harenberg A, de Montfort A, Jantet-Blaudez F, Bonaparte M, Boudet F, Saville M, Jackson N, Guy B. 2016. Cytokine profile of children hospitalized with virologically-confirmed dengue during two phase III vaccine efficacy trials. PLoS Negl Trop Dis, 10: e0004830.CrossRefPubMedPubMedCentralGoogle Scholar
Holmes EC and Burch SS (2000) The causes and consequences of genetic variation in dengue virus. Trends Microbiol, 8: 74–77.CrossRefPubMedGoogle Scholar
Luo L, Liang HY, Jing QL, He P, Yuan J, Di B, Bai ZJ, Wang YL, Zheng XL, Yang ZC. 2013. Molecular characterization of the envelope gene of dengue virus type 3 newly isolated in Guangzhou, China, during 2009–2010. Int J Infect Dis, 17: e498–e504.CrossRefPubMedGoogle Scholar
Mir D, Romero H, Fagundes DCL, Bello G. 2014. Spatiotemporal dynamics of DENV-2 Asian-American genotype lineages in the Americas. PLoS One, 9: e98519.CrossRefPubMedPubMedCentralGoogle Scholar
Quam MB, Sessions O, Kamaraj US, Rocklov J, Wilder-Smith A. 2016. Dissecting Japan's Dengue Outbreak in 2014. Am J Trop Med Hyg, 94: 409–412.CrossRefPubMedPubMedCentralGoogle Scholar
Rodenhuis-Zybert IA, Wilschut J, Smit JM. 2010. Dengue virus life cycle: viral and host factors modulating infectivity. Cell Mol Life Sci, 67: 2773–2786.CrossRefPubMedGoogle Scholar
Rohani A, Suzilah I, Malinda M, Anuar I, Mohd MI, Salmah MM, Topek O, Tanrang Y, Ooi SC, Rozilawati H, Lee HL. 2011. Aedes larval population dynamics and risk for dengue epidemics in Malaysia. Trop Biomed, 28: 237–248.PubMedGoogle Scholar
Sang S, Chen B, Wu H, Yang Z, Di B, Wang L, Tao X, Liu X, Liu Q. 2015. Dengue is still an imported disease in China: a case study in Guangzhou. Infect Genet Evol, 32: 178–190.CrossRefPubMedGoogle Scholar
Sang S, Gu S, Bi P, Yang W, Yang Z, Xu L, Yang J, Liu X, Jiang T, Wu H, Chu C, Liu Q. 2015. Predicting unprecedented dengue outbreak using imported cases and climatic factors in Guangzhou, 2014. PLoS Negl Trop Dis, 9: e0003808.CrossRefPubMedPubMedCentralGoogle Scholar
Sarfraz MS, Tripathi NK, Faruque FS, Bajwa UI, Kitamoto A, Souris M. 2014. Mapping urban and peri-urban breeding habitats of Aedes mosquitoes using a fuzzy analytical hierarchical process based on climatic and physical parameters. Geospat Health, 8: S685–S697.CrossRefPubMedGoogle Scholar
Wang B, Li Y, Feng Y, Zhou H, Liang Y, Dai J, Qin W, Hu Y, Wang Y, Zhang L, Baloch Z, Yang H, Xia X. 2015. Phylogenetic analysis of dengue virus reveals the high relatedness between imported and local strains during the 2013 dengue outbreak in Yunnan, China: a retrospective analysis. BMC Infect Dis, 15: 142.CrossRefPubMedPubMedCentralGoogle Scholar
WHO. 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control: New Edition. WHO Guidelines Approved by the Guidelines Review Committee World Health Organization, Geneva.Google Scholar
Wu W, Bai Z, Zhou H, Tu Z, Fang M, Tang B, Liu J, Liu L, Liu J, Chen W. 2011. Molecular epidemiology of dengue viruses in southern China from 1978 to 2006. Virol J, 8: 322.CrossRefPubMedPubMedCentralGoogle Scholar
Yang HM, Boldrini JL, Fassoni AC, Freitas LF, Gomez MC, de Lima KK, Andrade VR, Freitas AR. 2016. Fitting the incidence data from the city of Campinas, Brazil, based on dengue transmission modellings considering time-dependent entomological parameters. PLoS One, 11: e0152186.CrossRefPubMedPubMedCentralGoogle Scholar
Yang T, Lu L, Fu G, Zhong S, Ding G, Xu R, Zhu G, Shi N, Fan F, Liu Q. 2009. Epidemiology and vector efficiency during a dengue fever outbreak in Cixi, Zhejiang Province, China. J Vector Ecol, 34: 148–154.CrossRefPubMedGoogle Scholar
Yong YK, Thayan R, Chong HT, Tan CT, Sekaran SD. 2007. Rapid detection and serotyping of dengue virus by multiplex RT-PCR and real-time SYBR green RT-PCR. Singapore Med J, 48: 662–668.PubMedGoogle Scholar
Zellweger RM, Prestwood TR, Shresta S. 2010. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe, 7: 128–139.CrossRefPubMedPubMedCentralGoogle Scholar
Zhao H, Zhang FC, Zhu Q, Wang J, Hong WX, Zhao LZ, Deng YQ, Qiu S, Zhang Y, Cai WP, Cao WC, Qin CF. 2016. Epidemiological and virological characterizations of the 2014 dengue outbreak in Guangzhou, China. PLoS One, 11: e0156548.CrossRefPubMedPubMedCentralGoogle Scholar
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creative commons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
