Emergence, circulation, and spatiotemporal phylogenetic analysis of coxsackievirus a6- and coxsackievirus a10-associated hand, foot, and mouth disease infections from 2008 to 2012 in Shenzhen China

Journal of Clinical Microbiology

Volumn 51, Issue 11, 2013, Pages 3560-3566

  He, Ya Qing ^a   Chen, Long ^a,b   Xu, Wen Bo ^c   Yang, Hong ^a   Wang, Han Zhong ^d   Zong, Wen Ping ^a   Xian, Hui Xia ^a   Chen, Hui Ling ^a   Yao, Xiang Jie ^a   Hu, Zhang Li ^b   Luo, Min ^a   Zhang, Hai Long ^a   Ma, Han Wu ^a   Cheng, Jin Quan ^a   Feng, Qian Jin ^e   Zhao, De Jian ^a  

^a SHENZHEN CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^b SHENZHEN UNIVERSITY   (China)

^c CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^d WUHAN INSTITUTE OF VIROLOGY   (China)

^e SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

ARTICLE; CHINA; CONTROLLED STUDY; COXSACKIE VIRUS A; COXSACKIE VIRUS A10; COXSACKIE VIRUS A6; COXSACKIE VIRUS INFECTION; DISEASE SURVEILLANCE; FECES ANALYSIS; FEMALE; GENETIC RECOMBINATION; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HAND FOOT AND MOUTH DISEASE; HOSPITAL; HUMAN; MAJOR CLINICAL STUDY; MALE; MOLECULAR EVOLUTION; MUTATION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBSERVATIONAL STUDY; PHYLOGENY; PREVALENCE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PUBLIC HEALTH; REAL TIME POLYMERASE CHAIN REACTION; SPATIOTEMPORAL ANALYSIS; STRAIN DIFFERENCE; UNINDEXED SEQUENCE; VIRAL GENETICS; VIRUS DETECTION; VIRUS GENE; VIRUS MUTATION; VIRUS STRAIN; VP1 GENE;

CHILD, PRESCHOOL; CHINA; ENTEROVIRUS; EVOLUTION, MOLECULAR; FECES; FEMALE; GENOTYPE; HAND, FOOT AND MOUTH DISEASE; HUMANS; INFANT; MALE; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; MUTATION RATE; PHYLOGEOGRAPHY; POLYMERASE CHAIN REACTION; PREVALENCE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

EID: 84886554467     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.01231-13     Document Type: Article

References (35)

1. Palacios G, Oberste MS. 2005. Enteroviruses as agents of emerging infectious diseases. J. Neurovirol. 11:424-433.
2. Chang LY, Lin TY, Hsu KH, Huang YC, Lin KL, Hsueh C, Shih SR, Ning HC, Hwang MS, Wang HS, Lee CY. 1999. Clinical features and risk factors of pulmonary oedema after enterovirus-71-related hand, foot, and mouth disease. Lancet 354:1682-1686.
3. Shah VA, Chong CY, Chan KP, Ng W, Ling AE. 2003. Clinical characteristics of an outbreak of hand, foot and mouth disease in Singapore. Ann. Acad. Med. Singapore 32:381-387.
4. Tee KK, Lam TT, Chan YF, Bible JM, Kamarulzaman A, Tong CY, Takebe Y, Pybus OG. 2010. Evolutionary genetics of human enterovirus 71: origin, population dynamics, natural selection, and seasonal periodicity of the VP1 gene. J. Virol. 84:3339-3350.
5. Zheng ZM, He PJ, Caueffield D, Neumann M, Specter S, Baker CC, Bankowski MJ. 1995. Enterovirus 71 isolated from China is serologically similar to the prototype E71 BrCr strain but differs in the 5=-noncoding region. J. Med. Virol. 47:161-167.
6. Yang F, Ren L, Xiong Z, Li J, Xiao Y, Zhao R, He Y, Bu G, Zhou S, Wang J, Qi J. 2009. Enterovirus 71 outbreak in the People's Republic of China in 2008. J. Clin. Microbiol. 47:2351-2352.
7. Zhang Y, Tan XJ, Wang HY, Yan DM, Zhu SL, Wang DY, Ji F, Wang XJ, Gao YJ, Chen L, An HQ, Li DX, Wang SW, Xu AQ, Wang ZJ, Xu WB. 2009. An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. J. Clin. Virol. 44:262-267.
8. Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, Mao N, Xu S, Zhu S, Cui A, Zhang Y, Yan D, Li Q, Dong X, Zhang J, Zhao Y, Wan J, Feng Z, Sun J, Wang S, Li D, Xu W. 2010. An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol. J. 7:94. doi:10.1186 /1743-422X-7-94.
9. Wu Y, Yeo A, Phoon MC, Tan EL, Poh CL, Quak SH, Chow VT. 2010. The largest outbreak of hand; foot and mouth disease in Singapore in 2008: the role of enterovirus 71 and coxsackievirus A strains. Int. J. Infect. Dis. 14:e1076-e1081. doi:10.1016/j.ijid.2010.07.006.
10. Blomqvist S, Klemola P, Kaijalainen S, Paananen A, Simonen ML, Vuorinen T, Roivainen M. 2010. Co-circulation of coxsackieviruses A6 and A10 in hand, foot and mouth disease outbreak in Finland. J. Clin. Virol. 48:49-54.
11. Lo SH, Huang YC, Huang CG, Tsao KC, Li WC, Hsieh YC, Chiu CH, Lin TY. 2011. Clinical and epidemiologic features of coxsackievirus A6 infection in children in northern Taiwan between 2004 and 2009. J. Microbiol. Immunol. Infect. 44:252-257.
12. Mirand A, Henquell C, Archimbaud C, Ughetto S, Antona D, Bailly JL, Peigue-Lafeuille H. 2011. Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infections in 2010, France: a large citywide, prospective observational study. Clin. Microbiol. Infect. 18:E110-E118. doi:10.1111/j.1469-0691.2012.03789.x.
13. Wei SH, Huang YP, Liu MC, Tsou TP, Lin HC, Lin TL, Tsai CY, Chao YN, Chang LY, Hsu CM. 2011. An outbreak of coxsackievirus A6 hand, foot, and mouth disease associated with onychomadesis in Taiwan, 2010. BMC Infect. Dis. 11:346. doi:10.1186/1471-2334-11-346.
14. Yamashita T, Ito M, Taniguchi A, Sakae K. 2005. Prevalence of coxsackievirus A5, A6, and A10 in patients with herpangina in Aichi Prefecture, 2005. Jpn. J. Infect. Dis. 58:390-391.
15. Bracho MA, González-Candelas F, Valero A, Córdoba J, Salazar A. 2011. Enterovirus co-infections and onychomadesis after hand, foot, and mouth disease, Spain, 2008. Emerg. Infect. Dis. 17:2223-2231.
16. Fujimoto T, Iizuka S, Enomoto M, Abe K, Yamashita K, Hanaoka N, Okabe N, Yoshida H, Yasui Y, Kobayashi M, Fujii Y, Tanaka H, Yamamoto M, Shimizu H. 2012. Hand, foot, and mouth disease caused by coxsackievirus A6, Japan, 2011. Emerg. Infect. Dis. 18:337-339.
17. Oberste MS, Peñaranda S, Rogers SL, Henderson E, Nix WA. 2010. Comparative evaluation of Taqman real-time PCR and semi-nested VP1 PCR for detection of enteroviruses in clinical specimens. J. Clin. Virol. 49:73-74.
18. Nix WA, Oberste MS, Pallansch MA. 2006. Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J. Clin. Microbiol. 44:2698-2704.
19. Mirand A, Schuffenecker I, Henquell C, Billaud G, Jugie G, Falcon D, Mahul A, Archimbaud C, Terletskaia-Ladwig E, Diedrich S, Huemer HP, Enders M, Lina B, Peigue-Lafeuille H, Bailly JL. 2010. Phylogenetic evidence for a recent spread of two populations of human enterovirus 71 in European countries. J. Gen. Virol. 91:2263-2277.
20. Mirand A, Henquell C, Archimbaud C, Chambon M, Charbonne F, Peigue-Lafeuille H, Bailly JL. 2008. Prospective identification of enteroviruses involved in meningitis in 2006 through direct genotyping in cerebrospinal fluid. J. Clin. Microbiol. 46:87-96.
21. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
22. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214. doi:10.1186/1471-2148-7 -214.
23. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88. doi:10.1371 /journal.pbio.0040088.
24. Hasegawa M, Kishino H, Yano T. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174.
25. RodrÍguez F, Oliver JL, MarÍn A, Medina JR. 1990. The general stochastic model of nucleotide substitution. J. Theor. Biol. 142:485-501.
26. Oberste MS, Maher K, Kilpatrick DR, Flemister MR, Brown BA, Pallansch MA. 1999. Typing of human enteroviruses by partial sequencing of VP1. J. Clin. Microbiol. 37:1288-1293.
27. Chen H, Liu Q, Wang D, Chen Y, Feng B, Li G, Yao W, Shu B, He Y. 2013. Surveillance and analysis of enteroviruses in water environments in Shenzhen from 2010 to 2011. Arch. Virol. 158:1343-1347.
28. McWilliam Leitch EC, Cabrerizo M, Cardosa J, Harvala H, Ivanova OE, Kroes AC, Lukashev A, Muir P, Odoom J, Roivainen M, Susi P, Trallero G, Evans DJ, Simmonds P. 2010. Evolutionary dynamics and temporal/geographical correlates of recombination in the human enterovirus echovirus types 9, 11, and 30. J. Virol. 4:9292-9300.
29. Chu PY, Lu PL, Tsai YL, Hsi E, Yao CY, Chen YH, Hsu LC, Wang SY, Wu HS, Lin YY, Su HJ, Lin KH. 2011. Spatiotemporal phylogenetic analysis and molecular characterization of coxsackievirus A4. Infect. Genet. Evol. 11:1426-1435.
30. Bailly JL, Mirand A, Henquell C, Archimbaud C, Chambon M, Regagnon C, Charbonné F, Peigue-Lafeuille H. 2011. Repeated genomic transfers from echovirus 30 to echovirus 6 lineages indicate co-divergence between co-circulating populations of the two human enterovirus serotypes. Infect. Genet. Evol. 11:276-289.
31. Gullberg M, Tolf C, Jonsson N, Mulders MN, Savolainen-Kopra C, Hovi T, Van Ranst M, Lemey P, Hafenstein S, Lindberg AM. 2010. Characterization of a putative ancestor of coxsackievirus B5. J. Virol. 84: 9695-9708.
32. Drake JW, Charlesworth B, Charlesworth D, Crow JF. 1998. Rates of spontaneous mutation. Genetics 148:1667-1686.
33. Hu YF, Yang F, Du J, Dong J, Zhang T, Wu ZQ, Xue Y, Jin Q. 2011. Complete genome analysis of coxsackievirus A2, A4, A5, and A10 strains isolated from hand, foot, and mouth disease patients in China revealing frequent recombination of human enterovirus A. J. Clin. Microbiol. 49: 2426-2434.
34. Oberste MS, Maher K, Pallansch MA. 2004. Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J. Virol. 78:855-867.
35. Wu W, Xu WB, Chen L, Chen HL, Liu Q, Wang DL, Chen YJ, Yao W, Li G, Feng B, Shu BH, Zhou YK, He YQ. 2013. Molecular identification and analysis of human enteroviruses isolated from healthy children in Shenzhen, China from 2010 to 2011. PLoS One 8(6):e64889. doi:10.1371 /journal.pone.0064889.