Characterization of coxsackievirus A6-and enterovirus 71-associated hand foot and mouth disease in Beijing, China, from 2013 to 2015

Frontiers in Microbiology

Volumn 7, Issue MAR, 2016, Pages

  Li, Jie ^a,b   Sun, Ying ^b   Du, Yiwei ^b   Yan, Yuxiang ^a   Huo, Da ^b   Liu, Yuan ^b   Peng, Xiaoxia ^a   Yang, Yang ^b   Liu, Fen ^a   Lin, Changying ^b   Liang, Zhichao ^b   Jia, Lei ^b   Chen, Lijuan ^b   Wang, Quanyi ^b   He, Yan ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

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

Author keywords

Clinical features; Coxsackievirus A6; Enterovirus 71; Epidemic; Hand foot and mouth disease

Indexed keywords

ARTICLE; CHILD; CHINA; CLINICAL FEATURE; COXSACKIE VIRUS INFECTION; CRACKLE; DISEASE SEVERITY; ENTEROVIRUS INFECTION; FEMALE; FEVER; HAND FOOT AND MOUTH DISEASE; HUMAN; LYMPHOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; MENTAL DISEASE; NEUTROPHIL COUNT; PHYLOGENETIC TREE; PHYLOGENY; PRESCHOOL CHILD; PUPIL DISEASE; QUESTIONNAIRE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK FACTOR; SEROTYPE; TACHYCARDIA; VOMITING;

EID: 84964403634     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00391     Document Type: Article

References (49)

1. Acharya, R., Fry, E., Stuart, D., Fox, G., Rowlands, D., and Brown, F. (1989). The three-dimensional structure of foot-and-mouth disease virus at 2.9 A resolution. Nature 337, 709-716. doi: 10.1038/337709a0
2. Ben-Chetrit, E., Wiener-Well, Y., Shulman, L. M., Cohen, M. J., Elinav, H., Sofer, D., et al. (2014). Coxsackievirus A6-related hand foot and mouth disease: skin manifestations in a cluster of adult patients. J. Clin. Virol. 59, 201-203. doi: 10.1016/j.jcv.2013.12.012
3. Cardosa, M. J., Krishnan, S., Tio, P. H., Perera, D., and Wong, S. C. (1999). Isolation of subgenus B adenovirus during a fatal outbreak of enterovirus 71-associated hand, foot, and mouth disease in Sibu, Sarawak. Lancet 354, 987-991. doi: 10.1016/S0140-6736(98)11032-2
4. Chan, K. P., Goh, K. T., Chong, C. Y., Teo, E. S., Lau, G., and Ling, A. E. (2003). Epidemic hand, foot and mouth disease caused by human enterovirus 71, Singapore. Emerging Infect. Dis. 9, 78-85. doi: 10.3201/eid1301.020112
5. Chang, L. Y., Lin, T. Y., Huang, Y. C., Tsao, K. C., Shih, S. R., Kuo, M. L., et al. (1999). Comparison of enterovirus 71 and coxsackie-virus A16 clinical illnesses during the Taiwan enterovirus epidemic, 1998. Pediatr. Infect. Dis. J. 18, 1092-1096. doi: 10.1097/00006454-199912000-00013
6. Chang, S. C., Li, W. C., Chen, G. W., Tsao, K. C., Huang, C. G., Huang, Y. C., et al. (2012). Genetic characterization of enterovirus 71 isolated from patients with severe disease by comparative analysis of complete genomes. J. Med. Virol. 84, 931-939. doi: 10.1002/jmv.23287
7. Chong, P., Liu, C. C., Chow, Y. H., Chou, A. H., and Klein, M. (2015). Review of enterovirus 71 vaccines. Clin. Infect. Dis. 60, 797-803. doi: 10.1093/cid/ciu852
8. Chou, A. H., Liu, C. C., Chang, J. Y., Lien, S. P., Guo, M. S., Tasi, H. P., et al. (2012). Immunological evaluation and comparison of different EV71 vaccine candidates. Clin. Dev. Immunol. 2012:831282. doi: 10.1155/2012/831282
9. Feder, H. M., Bennett, N., and Modlin, J. F. (2014). Atypical hand, foot, and mouth disease: a vesiculobullous eruption caused by Coxsackie virus A6. Lancet Infect. Dis. 14, 83-86. doi: 10.1016/S1473-3099(13)70264-0
10. Fujimoto, T., Iizuka, S., Enomoto, M., Abe, K., Yamashita, K., Hanaoka, N., et al. (2012). Hand, foot, and mouth disease caused by coxsackievirus A6, Japan, 2011. Emerging Infect. Dis. 18, 337-339. doi: 10.3201/eid1802.111147
11. Gilbert, G. L., Dickson, K. E., Waters, M. J., Kennett, M. L., Land, S. A., and Sneddon, M. (1988). Outbreak of enterovirus 71 infection in Victoria, Australia, with a high incidence of neurologic involvement. Pediatr. Infect. Dis. J. 7, 484-488. doi: 10.1097/00006454-198807000-00007
12. Guimbao, J., Rodrigo, P., Alberto, M. J., and Omeñaca, M. (2010). Onychomadesis outbreak linked to hand, foot, and mouth disease, Spain, July 2008. Euro Surveill. 15, 1-5.
13. Haneke, E. (2010). Onychomadesis and hand, foot and mouth disease-is there a connection? Eurosurveillance 15, 2-2.
14. Ho, M., Chen, E. R., Hsu, K. H., Twu, S. J., Chen, K. T., Tsai, S. F., et al. (1999). An epidemic of enterovirus 71 infection in Taiwan. Taiwan enterovirus epidemic working group. New Engl. J. Med. 341, 929-935. doi: 10.1056/nejm199909233411301
15. Hongyan, G., Chengjie, M., Qiaozhi, Y., Wenhao, H., Juan, L., Lin, P., et al. (2014). Hand, foot and mouth disease caused by coxsackievirus A6, Beijing, 2013. Pediatr. Infect. Dis. J. 33, 1302-1303. doi: 10.1097/INF.0000000000000467
16. Hu, Y. Q., Xie, G. C., Li, D. D., Pang, L. L., Xie, J., Wang, P., et al. (2015). Prevalence of coxsackievirus A6 and enterovirus 71 in hand, foot and mouth disease in Nanjing, China in 2013. Pediatr. Infect. Dis. J. 34, 951-957. doi: 10.1097/INF.0000000000000794
17. Huang, W. C., Huang, L. M., Lu, C. Y., Cheng, A. L., and Chang, L. Y. (2013). Atypical hand-foot-mouth disease in children: a hospital-based prospective cohort study. Virol. J. 10:209. doi: 10.1186/1743-422X-10-209
18. Huang, Y., Zhou, Y., Lu, H., Yang, H., Feng, Q., Dai, Y., et al. (2015). Characterization of severe hand, foot, and mouth disease in Shenzhen, China, 2009-2013. J. Med. Virol. 87, 1471-1479. doi: 10.1002/jmv.24200
19. Hyypiä, T., Hovi, T., Knowles, N. J., and Stanway, G. (1997). Classification of enteroviruses based on molecular and biological properties. J. Gen. Virol. 78 (Pt 1), 1-11. doi: 10.1099/0022-1317-78-1-1
20. Iwai, M., Masaki, A., Hasegawa, S., Obara, M., Horimoto, E., Nakamura, K., et al. (2009). Genetic changes of coxsackievirus A16 and enterovirus 71 isolated from hand, foot, and mouth disease patients in Toyama, Japan between 1981 and 2007. Jpn. J. Infect. Dis. 62, 254-259.
21. Li, J. L., Yuan, J., Yang, F., Wu, Z. Q., Hu, Y. F., Xue, Y., et al. (2014). Epidemic characteristics of hand, foot, and mouth disease in southern China, 2013: coxsackievirus A6 has emerged as the predominant causative agent. J. Infect. 69, 299-303. doi: 10.1016/j.jinf.2014.04.001
22. Li, L., Yin, H., An, Z., and Feng, Z. (2015). Considerations for developing an immunization strategy with enterovirus 71 vaccine. Vaccine 33, 1107-1112. doi: 10.1016/j.vaccine.2014.10.081
23. Lo, S. H., Huang, Y. C., Huang, C. G., Tsao, K. C., Li, W. C., Hsieh, Y. C., et al. (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. doi: 10.1016/j.jmii.2011.01.031
24. Lu, J., Zeng, H., Zheng, H., Yi, L., Guo, X., Liu, L., et al. (2014). Hand, foot and mouth disease in Guangdong, China, in 2013: new trends in the continuing epidemic. Clin. Microbiol. Infect. 20, O442-O445. doi: 10.1111/1469-0691.12468
25. Minor, P. D. (1990). Antigenic structure of picornaviruses. Curr. Top. Microbiol. Immunol. 161, 121-154. doi: 10.1007/978-3-642-75602-3_5
26. Nix, W. A., Oberste, M. S., and Pallansch, M. A. (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. doi: 10.1128/JCM.00542-06
27. Oberste, M. S., Maher, K., Kilpatrick, D. R., Flemister, M. R., Brown, B. A., and Pallansch, M. A. (1999a). Typing of human enteroviruses by partial sequencing of VP1. J. Clin. Microbiol. 37, 1288-1293.
28. Oberste, M. S., Maher, K., Kilpatrick, D. R., and Pallansch, M. A. (1999b). Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J. Virol. 73, 1941-1948.
29. Osterback, R., Vuorinen, T., Linna, M., Susi, P., Hyypia, T., and Waris, M. (2010). Coxsackievirus A6 and hand, foot, and mouth disease, Finland. Emerging Infect. Dis. 15, 1485-1488. doi: 10.3201/eid1509.090438
30. Pallansch Ma, R. R. (2001). Enteroviruses: Polioviruses, Coxsackieviruses, Echoviruses and Newer Enteroviruses. Philadelphia, PA: Lippincott Williams and Wilkins.
31. Pan, H., Zheng, Y. X., Mao, S. H., Hu, J. Y., Zheng, Y., Li, J., et al. (2012). A case-control study on risk factors that associated with severe hand-foot-mouth disease in Shanghai. Zhonghua Liu Xing Bing Xue Za Zhi 33, 763-767. doi: 10.3760/cma.j.issn.0254-6450.2012.08.002
32. Perera, D., Yusof, M. A., Podin, Y., Ooi, M. H., Thao, N. T., Wong, K. K., et al. (2007). Molecular phylogeny of modern coxsackievirus A16. Arch. Virol. 152, 1201-1208. doi: 10.1007/s00705-006-0934-5
33. Pöyry, T., Kinnunen, L., Hyypia, T., Brown, B., Horsnell, C., Hovi, T., et al. (1996). Genetic and phylogenetic clustering of enteroviruses. J. Gen. Virol. 77 (Pt 8), 1699-1717. doi: 10.1099/0022-1317-77-8-1699
34. Puenpa, J., Chieochansin, T., Linsuwanon, P., Korkong, S., Thongkomplew, S., Vichaiwattana, P., et al. (2013). Hand, foot, and mouth disease caused by coxsackievirus A6, Thailand, 2012. Emerging Infect. Dis. 19, 641-643. doi: 10.3201/eid1904.121666
35. Sinclair, C., Gaunt, E., Simmonds, P., Broomfield, D., Nwafor, N., Wellington, L., et al. (2014). Atypical hand, foot, and mouth disease associated with coxsackievirus A6 infection, Edinburgh, United Kingdom, January to February 2014. Euro Surveill. 19, 20745. doi: 10.2807/1560-7917.ES2014.19.12.20745
36. Tan, X., Li, L., Zhang, B., Jorba, J., Su, X., Ji, T., et al. (2015). Molecular epidemiology of coxsackievirus A6 associated with outbreaks of hand, foot, and mouth disease in Tianjin, China, in 2013. Arch. Virol. 160, 1097-1104. doi: 10.1007/s00705-015-2340-3
37. Tu, P. V., Thao, N. T., Perera, D., Huu, T. K., Tien, N. T., Thuong, T. C., et al. (2007). Epidemiologic and virologic investigation of hand, foot, and mouth disease, southern Vietnam, 2005. Emerging Infect. Dis. 13, 1733-1741. doi: 10.3201/eid1311.070632
38. Wang, S. M., Lei, H. Y., Huang, K. J., Wu, J. M., Wang, J. R., Yu, C. K., et al. (2003). Pathogenesis of enterovirus 71 brainstem encephalitis in pediatric patients: roles of cytokines and cellular immune activation in patients with pulmonary edema. J. Infect. Dis. 188, 564-570. doi: 10.1086/376998
39. Wang, S. M., and Liu, C. C. (2014). Update of enterovirus 71 infection: epidemiology, pathogenesis and vaccine. Expert Rev. Anti Infect. Ther. 12, 447-456. doi: 10.1586/14787210.2014.895666
40. Wei, S. H., Huang, Y. P., Liu, M. C., Tsou, T. P., Lin, H. C., Lin, T. L., et al. (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
41. Wu, Y., Yeo, A., Phoon, M. C., Tan, E. L., Poh, C. L., Quak, S. H., et al. (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
42. Xing, W., Liao, Q., Viboud, C., Zhang, J., Sun, J., Wu, J. T., et al. (2014). Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect. Dis. 14, 308-318. doi: 10.1016/S1473-3099(13)70342-6
43. Yang, F., Yuan, J., Wang, X., Li, J., Du, J., Su, H., et al. (2014). Severe hand, foot, and mouth disease and coxsackievirus A6-Shenzhen, China. Clin. Infect. Dis. 59, 1504-1505. doi: 10.1093/cid/ciu624
44. Zeng, H., Lu, J., Zheng, H., Yi, L., Guo, X., Liu, L., et al. (2015). The epidemiological study of coxsackievirus A6 revealing hand, foot and mouth disease epidemic patterns in Guangdong, China. Sci. Rep. 5, 10550. doi: 10.1038/srep10550
45. Zhang, Y., Tan, X. J., Wang, H. Y., Yan, D. M., Zhu, S. L., Wang, D. Y., et al. (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. doi: 10.1016/j.jcv.2009.02.002
46. Zhang, Y., Wang, J., Guo, W., Wang, H., Zhu, S., Wang, D., et al. (2011). Emergence and transmission pathways of rapidly evolving evolutionary branch C4a strains of human enterovirus 71 in the Central Plain of China. PLoS ONE 6:e27895. doi: 10.1371/journal.pone.0027895
47. Zhang, Y., Zhu, Z., Yang, W., Ren, J., Tan, X., Wang, Y., et al. (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
48. Zhu, F., Xu, W., Xia, J., Liang, Z., Liu, Y., Zhang, X., et al. (2014). Efficacy, safety, and immunogenicity of an enterovirus 71 vaccine in China. N. Engl. J. Med. 370, 818-828. doi: 10.1056/NEJMoa1304923
49. Zhu, F. C., Meng, F. Y., Li, J. X., Li, X. L., Mao, Q. Y., Tao, H., et al. (2013). Efficacy, safety, and immunology of an inactivated alum-adjuvant enterovirus 71 vaccine in children in China: a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 381, 2024-2032. doi: 10.1016/S0140-6736(13)61049-1