Molecular epidemiology of Japanese encephalitis in northern Vietnam, 1964–2011: genotype replacement
Tóm tắt
Japanese encephalitis virus (JEV) is an arthropod-borne virus causing serious public health issues in Asia. JEV consists of five genotypes and recent studies have shown the emergence of JEV genotype I (GI) and its replacement of genotype III (GIII). Using an archival JEV collection, we investigated the molecular evolution of JEV in Vietnam over the last 48 years (1964–2012) in humans, mosquitoes, and pigs, within the global context. The nine JEV isolates from humans, pigs, and mosquitoes sequenced in this study and 29 sequences available in GenBank were used to analyze the envelope (E) protein of the Vietnamese JEVs. A collection of 225 cerebrospinal fluid specimens from patients with suspected Japanese encephalitis (JE) was also tested and genotyped with real-time RT–PCR. The 38 E genes identified with sequencing and nine Vietnamese JEV strains genotyped with real-time RT–PCR, belonging to two lineages, evolved in accordance with those in the rest of the world. The first GIII strain was detected in humans in Vietnam in 1964, and in mosquitoes in 1979, whereas GI strains were first detected in humans and mosquitoes in 1990 and 1994, respectively. After 2004, GI was the only genotype detected in Vietnam, demonstrating that the GIIII strains had been displaced by GI strains. Five haplotypes were identified in the Vietnamese JEVs, with SKSS predominant. The S123N and S123R substitutions in the E protein were already present in the Vietnamese JEVs. This study describes the long evolutionary history of JEV in Vietnam over 34 years, which correlates well with the global evolution of JEV. The Vietnamese GIII strains have been replaced by GI strains in mosquitoes, pigs, and humans. The predominant haplotypes of the Vietnamese strains support this genotype displacement in Vietnam. Further surveillance is required to confirm the disappearance of the GIII strains in nature and the emergence of new pathogens causing encephalitis in Vietnam, after the long-term use of JEV vaccines in that country.
Tài liệu tham khảo
Erlanger TE, Weiss S, Keiser J, Utzinger J, Wiedenmayer K. Past, present, and future of Japanese encephalitis. Emerg Infect Dis. 2009;15(1):1–7.
Solomon T. Control of Japanese encephalitis–within our grasp? N Engl J Med. 2006;355(9):869–71.
Campbell GL, Hills SL, Fischer M, Jacobson JA, Hoke CH, Hombach JM, et al. Estimated global incidence of Japanese encephalitis: a systematic review. Bull World Health Organ. 2011;89(10):766–74. 774A-774E.
Lindenbach B, Murray C, Thiel H, Rice C. Flaviviridae. Field Virol. 2013;1:712–46.
Williams DT, Wang LF, Daniels PW, Mackenzie JS. Molecular characterization of the first Australian isolate of Japanese encephalitis virus, the FU strain. J Gen Virol. 2000;81(Pt 10):2471–80.
Schuh AJ, Li L, Tesh RB, Innis BL, Barrett AD. Genetic characterization of early isolates of Japanese encephalitis virus: genotype II has been circulating since at least 1951. J Gen Virol. 2010;91(Pt 1):95–102.
Uchil PD, Satchidanandam V. Phylogenetic analysis of Japanese encephalitis virus: envelope gene based analysis reveals a fifth genotype, geographic clustering, and multiple introductions of the virus into the Indian subcontinent. Am J Trop Med Hyg. 2001;65(3):242–51.
Schuh AJ, Ward MJ, Leigh Brown AJ, Barrett AD. Dynamics of the emergence and establishment of a newly dominant genotype of Japanese encephalitis virus throughout Asia. J Virol. 2014;88(8):4522–32.
Yun SM, Cho JE, Ju YR, Kim SY, Ryou J, Han MG, et al. Molecular epidemiology of Japanese encephalitis virus circulating in South Korea, 1983-2005. Virol J. 2010;7:127.
Tang WF, Ogawa M, Eshita Y, Aono H, Makino Y. Molecular evolution of Japanese encephalitis virus isolates from swine in Oita, Japan during 1980-2009. Infect Genet Evol. 2010;10(2):329–36.
Ma SP, Yoshida Y, Makino Y, Tadano M, Ono T, Ogawa M. Short report: a major genotype of Japanese encephalitis virus currently circulating in Japan. Am J Trop Med Hyg. 2003;69(2):151–4.
Wang HY, Takasaki T, Fu SH, Sun XH, Zhang HL, Wang ZX, et al. Molecular epidemiological analysis of Japanese encephalitis virus in China. J Gen Virol. 2007;88(Pt 3):885–94.
Nga PT, del Carmen Parquet M, Cuong VD, Ma SP, Hasebe F, Inoue S, et al. Shift in Japanese encephalitis virus (JEV) genotype circulating in northern Vietnam: implications for frequent introductions of JEV from Southeast Asia to East Asia. J Gen Virol. 2004;85(Pt 6):1625–31.
Han N, Adams J, Chen P, Guo ZY, Zhong XF, Fang W, et al. Comparison of genotypes I and III in Japanese encephalitis virus reveals distinct differences in their genetic and host diversity. J Virol. 2014;88(19):11469–79.
Huong VT, Ha DQ, Deubel V. Genetic study of Japanese encephalitis viruses from Vietnam. Am J Trop Med Hyg. 1993;49(5):538–44.
Kuno G. Universal diagnostic RT-PCR protocol for arboviruses. J Virol Methods. 1998;72(1):27–41.
Yen NT, Duffy MR, Hong NM, Hien NT, Fischer M, Hills SL. Surveillance for Japanese encephalitis in Vietnam, 1998-2007. Am J Trop Med Hyg. 2010;83(4):816–9.
Do PL, Nga PT, Trang BM. Development of realtime RT - PCR in detection and differentiation Japanese encephalitis virus genotype GI and GIII. Vietnam J Pre Med. 2013;11(147):31–5.
Nam JH, Chae SL, Won SY, Kim EJ, Yoon KS, Kim BI, et al. Short report: genetic heterogeneity of Japanese encephalitis virus assessed via analysis of the full-length genome sequence of a Korean isolate. Am J Trop Med Hyg. 2001;65(4):388–92.
Fulmali PV, Sapkal GN, Athawale S, Gore MM, Mishra AC, Bondre VP. Introduction of Japanese encephalitis virus genotype I, India. Emerg Infect Dis. 2011;17(2):319–21.
Pyke AT, Williams DT, Nisbet DJ, van den Hurk AF, Taylor CT, Johansen CA, et al. The appearance of a second genotype of Japanese encephalitis virus in the Australasian region. Am J Trop Med Hyg. 2001;65(6):747–53.
Fan JM, Luo J, Chen L, Teng M, Bu D, Wang FY, et al. Genetic analysis of strains of Japanese Encephalitis Virus isolated from swine in central China. Virus Genes. 2010;40(3):357–61.
Nam JH, Chung YJ, Ban SJ, Kim EJ, Park YK, Cho HW. Envelope gene sequence variation among Japanese encephalitis viruses isolated in Korea. Acta Virol. 1996;40(5–6):303–9.
Tsuchie H, Oda K, Vythilingam I, Thayan R, Vijayamalar B, Sinniah M, et al. Genotypes of Japanese encephalitis virus isolated in three states in Malaysia. Am J Trop Med Hyg. 1997;56(2):153–8.
Ali A, Igarashi A, Paneru LR, Hasebe F, Morita K, Takagi M, et al. Characterization of two Japanese encephalitis virus strains isolated in Thailand. Arch Virol. 1995;140(9):1557–75.
Kiwanuka N, Sanders EJ, Rwaguma EB, Kawamata J, Ssengooba FP, Najjemba R, et al. O’nyong-nyong fever in south-central Uganda, 1996-1997: clinical features and validation of a clinical case definition for surveillance purposes. Clin Infect Dis. 1999;29(5):1243–50.
Vu TT, Holmes EC, Duong V, Nguyen TQ, Tran TH, Quail M, et al. Emergence of the Asian 1 genotype of dengue virus serotype 2 in viet nam: in vivo fitness advantage and lineage replacement in South-East Asia. PLoS Negl Trop Dis. 2010;4(7):e757.
Tajima S, Nerome R, Nukui Y, Kato F, Takasaki T, Kurane I. A single mutation in the Japanese encephalitis virus E protein (S123R) increases its growth rate in mouse neuroblastoma cells and its pathogenicity in mice. Virology. 2010;396(2):298–304.
Lee E, Hall RA, Lobigs M. Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J Virol. 2004;78(15):8271–80.
Nga PT, Parquet Mdel C, Lauber C, Parida M, Nabeshima T, Yu F, et al. Discovery of the first insect nidovirus, a missing evolutionary link in the emergence of the largest RNA virus genomes. PLoS Pathog. 2011;7(9):e1002215.
Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22(22):4673–80.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9.
Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25.