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Published in: BMC Infectious Diseases 1/2019

Open Access 01-12-2019 | Coxsackievirus | Research article

Two Coxsackievirus B3 outbreaks associated with hand, foot, and mouth disease in China and the evolutionary history worldwide

Authors: Zhenzhi Han, Yong Zhang, Keqiang Huang, Jianxing Wang, Huifang Tian, Yang Song, Qian Yang, Dongmei Yan, Shuangli Zhu, Mingxiao Yao, Xianjun Wang, Wenbo Xu

Published in: BMC Infectious Diseases | Issue 1/2019

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Abstract

Background

Coxsackievirus B3 (CV-B3) is usually associated with aseptic meningitis and myocarditis; however, the association between CV-B3 and hand, foot, and mouth disease (HFMD) has not been clearly demonstrated, and the phylogenetic dynamics and transmission history of CV-B3 have not been well summarized.

Method

Two HFMD outbreaks caused by CV-B3 were described in Hebei Province in 2012 and in Shandong Province in 2016 in China. To analyze the epidemiological features of two CV-B3 outbreaks, a retrospective analysis was conducted. All clinical specimens from CV-B3 outbreaks were collected and disposed according to the standard procedures supported by the WHO Global Poliovirus Specialized Laboratory. EV genotyping and phylogenetic analysis were performed to illustrate the genetic characteristics of CV-B3 in China and worldwide.

Results

Two transmissible lineages (lineage 2 and 3) were observed in Northern China, which acted as an important “reservoir” for the transmission of CV-B3. Sporadic exporting and importing of cases were observed in almost all regions. In addition, the global sequences of CV-B3 showed a tendency of geographic-specific clustering, indicating that geographic-driven adaptation plays a major role in the diversification and evolution of CV-B3.

Conclusions

Overall, our study indicated that CV-B3 is a causative agent of HFMD outbreak and revealed the phylogenetic dynamics of CV-B3 worldwide, as well as provided an insight on CV-B3 outbreaks for effective intervention and countermeasures.
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Literature
1.
go back to reference Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, Lindberg AM, Pallansch MA, Palmenberg AC, Reuter G, et al. ICTV virus taxonomy profile: Picornaviridae. J Gen Virol. 2017;98(10):2421–2.CrossRefPubMedPubMedCentral Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, Lindberg AM, Pallansch MA, Palmenberg AC, Reuter G, et al. ICTV virus taxonomy profile: Picornaviridae. J Gen Virol. 2017;98(10):2421–2.CrossRefPubMedPubMedCentral
2.
go back to reference Sin J, Mangale V, Thienphrapa W, Gottlieb RA, Feuer R. Recent progress in understanding coxsackievirus replication, dissemination, and pathogenesis. Virology. 2015;484:288–304.CrossRefPubMed Sin J, Mangale V, Thienphrapa W, Gottlieb RA, Feuer R. Recent progress in understanding coxsackievirus replication, dissemination, and pathogenesis. Virology. 2015;484:288–304.CrossRefPubMed
3.
go back to reference Lindberg AM, Stålhandske POK, Pettersson U. Genome of coxsackievirus B3. Virology. 1987;156(1):50–63.CrossRefPubMed Lindberg AM, Stålhandske POK, Pettersson U. Genome of coxsackievirus B3. Virology. 1987;156(1):50–63.CrossRefPubMed
4.
go back to reference Lee CJ, Huang YC, Yang S, Tsao KC, Chen CJ, Hsieh YC, Chiu CH, Lin TY. Clinical features of coxsackievirus A4, B3 and B4 infections in children. PLoS One. 2014;9(2):e87391.CrossRefPubMedPubMedCentral Lee CJ, Huang YC, Yang S, Tsao KC, Chen CJ, Hsieh YC, Chiu CH, Lin TY. Clinical features of coxsackievirus A4, B3 and B4 infections in children. PLoS One. 2014;9(2):e87391.CrossRefPubMedPubMedCentral
5.
go back to reference Chu P, Ke G, Chen Y, Lu P, Chen H, Lee M, Chen B, Huang T, Li Y, Chou L, et al. Molecular epidemiology of Coxsackievirus B3. Infect Genet Evol. 2010;10(6):777–84.CrossRefPubMed Chu P, Ke G, Chen Y, Lu P, Chen H, Lee M, Chen B, Huang T, Li Y, Chou L, et al. Molecular epidemiology of Coxsackievirus B3. Infect Genet Evol. 2010;10(6):777–84.CrossRefPubMed
6.
go back to reference Wu Z, Du J, Zhang T, Xue Y, Yang F, Jin Q. Recombinant human Coxsackievirus B3 from children with acute myocarditis in China. J Clin Microbiol. 2013;51(9):3083–6.CrossRefPubMedPubMedCentral Wu Z, Du J, Zhang T, Xue Y, Yang F, Jin Q. Recombinant human Coxsackievirus B3 from children with acute myocarditis in China. J Clin Microbiol. 2013;51(9):3083–6.CrossRefPubMedPubMedCentral
7.
go back to reference Gao F, Bian L, Mao Q, Chen P, Yao X, Li J, Zhu F, Liang Z. An epidemic of coxsackievirus B3 infection in infants and children in Jiangsu Province, China: a prospective cohort study. Arch Virol. 2016;161(7):1945–7.CrossRefPubMed Gao F, Bian L, Mao Q, Chen P, Yao X, Li J, Zhu F, Liang Z. An epidemic of coxsackievirus B3 infection in infants and children in Jiangsu Province, China: a prospective cohort study. Arch Virol. 2016;161(7):1945–7.CrossRefPubMed
8.
go back to reference Tao Z, Li B, Xu A, Liu Y, Song L, Wang S, Xiong P, Lin X, Song Y. Seroprevalence of coxsackievirus B3 in Yantai, China. Jpn J Infect Dis. 2013;66(6):537–8.CrossRefPubMed Tao Z, Li B, Xu A, Liu Y, Song L, Wang S, Xiong P, Lin X, Song Y. Seroprevalence of coxsackievirus B3 in Yantai, China. Jpn J Infect Dis. 2013;66(6):537–8.CrossRefPubMed
9.
go back to reference Chitambar SD, Yergolkar P, Laxmivandana R, Cherian SS. Genomic characterization of coxsackievirus type B3 strains associated with acute flaccid paralysis in South-Western India. J Gen Virol. 2016;97(3):694–705.CrossRefPubMed Chitambar SD, Yergolkar P, Laxmivandana R, Cherian SS. Genomic characterization of coxsackievirus type B3 strains associated with acute flaccid paralysis in South-Western India. J Gen Virol. 2016;97(3):694–705.CrossRefPubMed
10.
go back to reference Calderón KI, Díaz-de Cerio M, Otero A, Muñoz-Almagro C, Rabella N, Martínez-Rienda I, Moreno-Docón A, Trallero G, Cabrerizo M. Molecular epidemiology of coxsackievirus B3 infection in Spain, 2004-2014. Arch Virol. 2016;161(5):1365–70.CrossRefPubMed Calderón KI, Díaz-de Cerio M, Otero A, Muñoz-Almagro C, Rabella N, Martínez-Rienda I, Moreno-Docón A, Trallero G, Cabrerizo M. Molecular epidemiology of coxsackievirus B3 infection in Spain, 2004-2014. Arch Virol. 2016;161(5):1365–70.CrossRefPubMed
11.
go back to reference Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA. Enterovirus surveillance-United States, 1970-2005. MMWR Surveill Summ. 2006;55(8):1–20.PubMed Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA. Enterovirus surveillance-United States, 1970-2005. MMWR Surveill Summ. 2006;55(8):1–20.PubMed
12.
go back to reference Antona D, Lévêque N, Chomel JJ, Dubrou S, Lévy-Bruhl D, Lina B. Surveillance of enteroviruses in France, 2000–2004. Eur J Clin Microbiol. 2007;26(6):403–12.CrossRef Antona D, Lévêque N, Chomel JJ, Dubrou S, Lévy-Bruhl D, Lina B. Surveillance of enteroviruses in France, 2000–2004. Eur J Clin Microbiol. 2007;26(6):403–12.CrossRef
13.
go back to reference Roth B, Enders M, Arents A, Pfitzner A, Terletskaia-Ladwig E. Epidemiologic aspects and laboratory features of enterovirus infections in Western Germany, 2000–2005. J Med Virol. 2007;79(7):956–62.CrossRefPubMed Roth B, Enders M, Arents A, Pfitzner A, Terletskaia-Ladwig E. Epidemiologic aspects and laboratory features of enterovirus infections in Western Germany, 2000–2005. J Med Virol. 2007;79(7):956–62.CrossRefPubMed
14.
go back to reference Wong AH, Lau CS, Cheng PKC, Ng AYY, Lim WWL. Coxsackievirus B3-associated aseptic meningitis: An emerging infection in Hong Kong. J Med Virol. 2011;83(3):483–9.CrossRefPubMed Wong AH, Lau CS, Cheng PKC, Ng AYY, Lim WWL. Coxsackievirus B3-associated aseptic meningitis: An emerging infection in Hong Kong. J Med Virol. 2011;83(3):483–9.CrossRefPubMed
15.
go back to reference Zhang Y, Tan X, Cui A, Mao N, Xu S, Zhu Z, Zhou J, Shi J, Zhao Y, Wang X, et al. Complete genome analysis of the C4 subgenotype strains of enterovirus 71: predominant recombination C4 viruses persistently circulating in China for 14 years. PLoS One. 2013;8(2):e56341.CrossRefPubMedPubMedCentral Zhang Y, Tan X, Cui A, Mao N, Xu S, Zhu Z, Zhou J, Shi J, Zhao Y, Wang X, et al. Complete genome analysis of the C4 subgenotype strains of enterovirus 71: predominant recombination C4 viruses persistently circulating in China for 14 years. PLoS One. 2013;8(2):e56341.CrossRefPubMedPubMedCentral
16.
go back to reference Zhang Y, Wang D, Yan D, Zhu S, Liu J, Wang H, Zhao S, Yu D, Nan L, An J, et al. Molecular evidence of persistent epidemic and evolution of subgenotype B1 coxsackievirus A16-associated hand, foot, and mouth disease in China. J Clin Microbiol. 2010;48(2):619–22.CrossRefPubMed Zhang Y, Wang D, Yan D, Zhu S, Liu J, Wang H, Zhao S, Yu D, Nan L, An J, et al. Molecular evidence of persistent epidemic and evolution of subgenotype B1 coxsackievirus A16-associated hand, foot, and mouth disease in China. J Clin Microbiol. 2010;48(2):619–22.CrossRefPubMed
17.
go back to reference Song Y, Zhang Y, Ji T, Gu X, Yang Q, Zhu S, Xu W, Xu Y, Shi Y, Huang X, et al. Persistent circulation of Coxsackievirus A6 of genotype D3 in mainland of China between 2008 and 2015. Sci Rep. 2017;7(1):5491.CrossRefPubMedPubMedCentral Song Y, Zhang Y, Ji T, Gu X, Yang Q, Zhu S, Xu W, Xu Y, Shi Y, Huang X, et al. Persistent circulation of Coxsackievirus A6 of genotype D3 in mainland of China between 2008 and 2015. Sci Rep. 2017;7(1):5491.CrossRefPubMedPubMedCentral
18.
go back to reference Mizuta K, Abiko C, Murata T, Matsuzaki Y, Itagaki T, Sanjoh K, Sakamoto M, Hongo S, Murayama S, Hayasaka K. Frequent importation of enterovirus 71 from surrounding countries into the local community of Yamagata, Japan, between 1998 and 2003. J Clin Microbiol. 2005;43(12):6171–5.CrossRefPubMedPubMedCentral Mizuta K, Abiko C, Murata T, Matsuzaki Y, Itagaki T, Sanjoh K, Sakamoto M, Hongo S, Murayama S, Hayasaka K. Frequent importation of enterovirus 71 from surrounding countries into the local community of Yamagata, Japan, between 1998 and 2003. J Clin Microbiol. 2005;43(12):6171–5.CrossRefPubMedPubMedCentral
19.
go back to reference Ding X, Nie K, Shi L, Zhang Y, Guan L, Zhang D, Qi S, Ma X. Improved detection limit in rapid detection of human enterovirus 71 and coxsackievirus A16 by a novel reverse transcription-isothermal multiple-self-matching-initiated amplification assay. J Clin Microbiol. 2014;52(6):1862–70.CrossRefPubMedPubMedCentral Ding X, Nie K, Shi L, Zhang Y, Guan L, Zhang D, Qi S, Ma X. Improved detection limit in rapid detection of human enterovirus 71 and coxsackievirus A16 by a novel reverse transcription-isothermal multiple-self-matching-initiated amplification assay. J Clin Microbiol. 2014;52(6):1862–70.CrossRefPubMedPubMedCentral
20.
go back to reference Puenpa J, Vongpunsawad S, Österback R, Waris M, Eriksson E, Albert J, Midgley S, Fischer TK, Eis-Hübinger AM, Cabrerizo M, et al. Molecular epidemiology and the evolution of human coxsackievirus A6. J Gen Virol. 2016;97(12):3225–31.CrossRefPubMed Puenpa J, Vongpunsawad S, Österback R, Waris M, Eriksson E, Albert J, Midgley S, Fischer TK, Eis-Hübinger AM, Cabrerizo M, et al. Molecular epidemiology and the evolution of human coxsackievirus A6. J Gen Virol. 2016;97(12):3225–31.CrossRefPubMed
21.
go back to reference Wu Y, Yeo A, Phoon MC, Tan EL, Poh CL, Quak SH, Chow VT. 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. 2010;14(12):e1076–81.CrossRefPubMed Wu Y, Yeo A, Phoon MC, Tan EL, Poh CL, Quak SH, Chow VT. 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. 2010;14(12):e1076–81.CrossRefPubMed
22.
go back to reference Mirand A, le Sage FV, Pereira B, Cohen R, Levy C, Archimbaud C, Peigue-Lafeuille H, Bailly J, Henquell C. Ambulatory pediatric surveillance of hand, foot and mouth disease as signal of an outbreak of Coxsackievirus A6 infections, France, 2014–2015. Emerg Infect Dis. 2016;22(11):1884–93.CrossRefPubMedPubMedCentral Mirand A, le Sage FV, Pereira B, Cohen R, Levy C, Archimbaud C, Peigue-Lafeuille H, Bailly J, Henquell C. Ambulatory pediatric surveillance of hand, foot and mouth disease as signal of an outbreak of Coxsackievirus A6 infections, France, 2014–2015. Emerg Infect Dis. 2016;22(11):1884–93.CrossRefPubMedPubMedCentral
23.
go back to reference Anh NT, Nhu LNT, Van HMT, Hong NTT, Thanh TT, Hang VTT, Ny NTH, Nguyet LA, Phuong TTL, Nhan LNT, et al. Emerging Coxsackievirus A6 causing hand, foot and mouth disease, Vietnam. Emerg Infect Dis. 2018;24(4):654–62.CrossRefPubMedPubMedCentral Anh NT, Nhu LNT, Van HMT, Hong NTT, Thanh TT, Hang VTT, Ny NTH, Nguyet LA, Phuong TTL, Nhan LNT, et al. Emerging Coxsackievirus A6 causing hand, foot and mouth disease, Vietnam. Emerg Infect Dis. 2018;24(4):654–62.CrossRefPubMedPubMedCentral
24.
go back to reference Tian H, Zhang Y, Sun Q, Zhu S, Li X, Pan Z, Xu W, Xu B. Prevalence of multiple enteroviruses associated with hand, foot, and mouth disease in Shijiazhuang City, Hebei province, China: outbreaks of coxsackieviruses a10 and b3. PLoS One. 2014;9(1):e84233.CrossRefPubMedPubMedCentral Tian H, Zhang Y, Sun Q, Zhu S, Li X, Pan Z, Xu W, Xu B. Prevalence of multiple enteroviruses associated with hand, foot, and mouth disease in Shijiazhuang City, Hebei province, China: outbreaks of coxsackieviruses a10 and b3. PLoS One. 2014;9(1):e84233.CrossRefPubMedPubMedCentral
25.
go back to reference Oberste MS, Maher K, Williams AJ, Dybdahl-Sissoko N, Brown BA, Gookin MS, Penaranda S, Mishrik N, Uddin M, Pallansch MA. Species-specific RT-PCR amplification of human enteroviruses: a tool for rapid species identification of uncharacterized enteroviruses. J Gen Virol. 2006;87(Pt 1:119–28.CrossRefPubMed Oberste MS, Maher K, Williams AJ, Dybdahl-Sissoko N, Brown BA, Gookin MS, Penaranda S, Mishrik N, Uddin M, Pallansch MA. Species-specific RT-PCR amplification of human enteroviruses: a tool for rapid species identification of uncharacterized enteroviruses. J Gen Virol. 2006;87(Pt 1:119–28.CrossRefPubMed
26.
go back to reference Kroneman A, Vennema H, Deforche K, V DAH, Penaranda S, Oberste MS, Vinje J, Koopmans M. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol. 2011;51(2):121–5.CrossRefPubMed Kroneman A, Vennema H, Deforche K, V DAH, Penaranda S, Oberste MS, Vinje J, Koopmans M. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol. 2011;51(2):121–5.CrossRefPubMed
27.
28.
go back to reference Nguyen L, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74.CrossRefPubMed Nguyen L, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74.CrossRefPubMed
29.
go back to reference Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–9.CrossRefPubMedPubMedCentral Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–9.CrossRefPubMedPubMedCentral
32.
go back to reference Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–42.CrossRefPubMedPubMedCentral Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–42.CrossRefPubMedPubMedCentral
33.
34.
35.
go back to reference Rieux A, Khatchikian CE. TipDatingBeast: an R package to assist the implementation of phylogenetic tip-dating tests usingbeast. Mol Ecol Resour. 2017;17(4):608–13.CrossRefPubMed Rieux A, Khatchikian CE. TipDatingBeast: an R package to assist the implementation of phylogenetic tip-dating tests usingbeast. Mol Ecol Resour. 2017;17(4):608–13.CrossRefPubMed
36.
go back to reference Pybus OG. The epidemiology and iatrogenic transmission of hepatitis C virus in Egypt: a Bayesian coalescent approach. Mol Biol Evol. 2003;20(3):381–7.CrossRefPubMed Pybus OG. The epidemiology and iatrogenic transmission of hepatitis C virus in Egypt: a Bayesian coalescent approach. Mol Biol Evol. 2003;20(3):381–7.CrossRefPubMed
37.
go back to reference Parker J, Rambaut A, Pybus OG. Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol. 2008;8(3):239–46.CrossRefPubMed Parker J, Rambaut A, Pybus OG. Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol. 2008;8(3):239–46.CrossRefPubMed
38.
39.
go back to reference Kosakovsky Pond SL, Frost SDW. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol. 2005;22(5):1208–22.CrossRefPubMed Kosakovsky Pond SL, Frost SDW. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol. 2005;22(5):1208–22.CrossRefPubMed
40.
go back to reference Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 2012;8(7):e1002764.CrossRefPubMedPubMedCentral Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 2012;8(7):e1002764.CrossRefPubMedPubMedCentral
41.
go back to reference Tao Z, Song Y, Li Y, Liu Y, Jiang P, Lin X, Liu G, Song L, Wang H, Xu A. Coxsackievirus B3, Shandong Province, China, 1990–2010. Emerg Infect Dis. 2012;18(11):1865–7.CrossRefPubMedPubMedCentral Tao Z, Song Y, Li Y, Liu Y, Jiang P, Lin X, Liu G, Song L, Wang H, Xu A. Coxsackievirus B3, Shandong Province, China, 1990–2010. Emerg Infect Dis. 2012;18(11):1865–7.CrossRefPubMedPubMedCentral
42.
go back to reference Huang Y, Lin T, Chen Y, Hsu C, Lin T, Wu H. Phylogenetic analysis and development of an immunofluorescence assay for untypeable strains of coxsackievirus B3. J Microbiol Immunol Infect. 2014;47(6):447–54.CrossRefPubMed Huang Y, Lin T, Chen Y, Hsu C, Lin T, Wu H. Phylogenetic analysis and development of an immunofluorescence assay for untypeable strains of coxsackievirus B3. J Microbiol Immunol Infect. 2014;47(6):447–54.CrossRefPubMed
43.
go back to reference Takahashi S, Liao Q, Van Boeckel TP, Xing W, Sun J, Hsiao VY, Metcalf CJE, Chang Z, Liu F, Zhang J, et al. Hand, foot, and mouth disease in China: modeling epidemic dynamics of Enterovirus serotypes and implications for vaccination. PLoS Med. 2016;13(2):e1001958.CrossRefPubMedPubMedCentral Takahashi S, Liao Q, Van Boeckel TP, Xing W, Sun J, Hsiao VY, Metcalf CJE, Chang Z, Liu F, Zhang J, et al. Hand, foot, and mouth disease in China: modeling epidemic dynamics of Enterovirus serotypes and implications for vaccination. PLoS Med. 2016;13(2):e1001958.CrossRefPubMedPubMedCentral
44.
go back to reference Huang J, Liao Q, Ooi MH, Cowling BJ, Chang Z, Wu P, Liu F, Li Y, Luo L, Yu S, et al. Epidemiology of recurrent hand, foot and mouth disease, China, 2008–2015. Emerg Infect Dis. 2018;24(3):432–42 Huang J, Liao Q, Ooi MH, Cowling BJ, Chang Z, Wu P, Liu F, Li Y, Luo L, Yu S, et al. Epidemiology of recurrent hand, foot and mouth disease, China, 2008–2015. Emerg Infect Dis. 2018;24(3):432–42
45.
go back to reference Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, Mao N, Xu S, Zhu S, Cui A, et al. An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol J. 2010;7:94.CrossRefPubMedPubMedCentral Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, Mao N, Xu S, Zhu S, Cui A, et al. An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol J. 2010;7:94.CrossRefPubMedPubMedCentral
46.
go back to reference Chen SP, Huang YC, Li WC, Chiu CH, Huang CG, Tsao KC, Lin TY. Comparison of clinical features between coxsackievirus A2 and enterovirus 71 during the enterovirus outbreak in Taiwan, 2008: a children's hospital experience. J Microbiol Immunol Infect. 2010;43(2):99–104.CrossRefPubMed Chen SP, Huang YC, Li WC, Chiu CH, Huang CG, Tsao KC, Lin TY. Comparison of clinical features between coxsackievirus A2 and enterovirus 71 during the enterovirus outbreak in Taiwan, 2008: a children's hospital experience. J Microbiol Immunol Infect. 2010;43(2):99–104.CrossRefPubMed
47.
go back to reference Nie K, Zhang Y, Luo L, Yang MJ, Hu XM, Wang M, Zhu SL, Han F, Xu WB, Ma XJ. Visual detection of human enterovirus 71 subgenotype C4 and Coxsackievirus A16 by reverse transcription loop-mediated isothermal amplification with the hydroxynaphthol blue dye. J Virol Methods. 2011;175(2):283–6.CrossRefPubMed Nie K, Zhang Y, Luo L, Yang MJ, Hu XM, Wang M, Zhu SL, Han F, Xu WB, Ma XJ. Visual detection of human enterovirus 71 subgenotype C4 and Coxsackievirus A16 by reverse transcription loop-mediated isothermal amplification with the hydroxynaphthol blue dye. J Virol Methods. 2011;175(2):283–6.CrossRefPubMed
48.
49.
go back to reference Hu YF, Yang F, Du J, Dong J, Zhang T, Wu ZQ, Xue Y, Jin Q. 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. 2011;49(7):2426–34.CrossRefPubMedPubMedCentral Hu YF, Yang F, Du J, Dong J, Zhang T, Wu ZQ, Xue Y, Jin Q. 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. 2011;49(7):2426–34.CrossRefPubMedPubMedCentral
50.
go back to reference Thoelen I, Lemey P, Van der Donck I, Beuselinck K, Lindberg AM, Van Ranst M. Molecular typing and epidemiology of enteroviruses identified from an outbreak of aseptic meningitis in Belgium during the summer of 2000. J Med Virol. 2003;70(3):420–9.CrossRefPubMed Thoelen I, Lemey P, Van der Donck I, Beuselinck K, Lindberg AM, Van Ranst M. Molecular typing and epidemiology of enteroviruses identified from an outbreak of aseptic meningitis in Belgium during the summer of 2000. J Med Virol. 2003;70(3):420–9.CrossRefPubMed
51.
go back to reference Lee ST, Ki CS, Lee NY. Molecular characterization of enteroviruses isolated from patients with aseptic meningitis in Korea, 2005. Arch Virol. 2007;152(5):963–70.CrossRefPubMed Lee ST, Ki CS, Lee NY. Molecular characterization of enteroviruses isolated from patients with aseptic meningitis in Korea, 2005. Arch Virol. 2007;152(5):963–70.CrossRefPubMed
52.
go back to reference Harvala H, Broberg E, Benschop K, Berginc N, Ladhani S, Susi P, Christiansen C, McKenna J, Allen D, Makiello P, et al. Recommendations for enterovirus diagnostics and characterisation within and beyond Europe. J Clin Virol. 2018;101:11–7.CrossRefPubMed Harvala H, Broberg E, Benschop K, Berginc N, Ladhani S, Susi P, Christiansen C, McKenna J, Allen D, Makiello P, et al. Recommendations for enterovirus diagnostics and characterisation within and beyond Europe. J Clin Virol. 2018;101:11–7.CrossRefPubMed
Metadata
Title
Two Coxsackievirus B3 outbreaks associated with hand, foot, and mouth disease in China and the evolutionary history worldwide
Authors
Zhenzhi Han
Yong Zhang
Keqiang Huang
Jianxing Wang
Huifang Tian
Yang Song
Qian Yang
Dongmei Yan
Shuangli Zhu
Mingxiao Yao
Xianjun Wang
Wenbo Xu
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2019
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-019-4107-z

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