Citation: Jiayu Wang, Jiajing Liu, Fanghao Fang, Jiajin Wu, Tianjiao Ji, Yuying Yang, Ling Liu, Chongshan Li, Wanju Zhang, Xi Zhang, Zheng Teng. Genomic surveillance of coxsackievirus A10 reveals genetic features and recent appearance of genogroup D in Shanghai, China, 2016-2020 .VIROLOGICA SINICA, 2022, 37(2) : 177-186.  http://dx.doi.org/10.1016/j.virs.2022.01.028

Genomic surveillance of coxsackievirus A10 reveals genetic features and recent appearance of genogroup D in Shanghai, China, 2016-2020

  • Coxsackievirus A10 (CVA10) is one of the major causative agents of hand, foot and mouth disease (HFMD). To investigate the epidemiological characteristics as well as genetic features of CVA10 currently circulating in Shanghai, China, we collected a total of 9,952 sporadic HFMD cases from January 2016 to December 2020. In the past five years, CVA10 was the fourth prevalent causatives associated with HFMD in Shanghai and the overall positive rate was 2.78%. The annual distribution experienced significant fluctuations over the past five years. In addition to entire VP1 sequencing, complete genome sequencing and recombination analysis of CVA10 isolates in Shanghai were further performed. A total of 64 near complete genomes and 11 entire VP1 sequences in this study combined with reference sequences publicly available were integrated into phylogenetic analysis. The CVA10 sequences in this study mainly belonged to genogroup C and presented 91%-100% nucleotide identity with other Chinese isolates based on VP1 region. For the first time, our study reported the appearance of CVA10 genogroup D in Chinese mainland, which had led to large-scale outbreaks in Europe previously. The recombination analysis showed the recombination break point located between 5,100 nt and 6,700 nt, which suggesting intertypic recombination with CVA16 genogroup D. To conclusion, CVA10 genogroup C was the predominant genogroup in Shanghai during 2016-2020. CVA10 recombinant genogroup D was firstly reported in circulating in Chinese mainland. Continuous surveillance is needed to better understand the evolution relationships and transmission pathways of CVA10 to help to guide disease control and prevention.

  • 加载中
  • 10.1016j.virs.2022.01.028-ESM.docx
    1. Blomqvist, S., Klemola, P., Kaijalainen, S., Paananen, A., Simonen, M.L., 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.

    2. Bracho, M.A., Gonzalez-Candelas, F., Valero, A., Cordoba, J., Salazar, A., 2011. Enterovirus co-infections and onychomadesis after hand, foot, and mouth disease, Spain, 2008. Emerg. Infect. Dis. 17, 2223-2231.

    3. Caro, V., Guillot, S., Delpeyroux, F., Crainic, R., 2001. Molecular strategy for 'serotyping' of human enteroviruses. J. Gen. Virol. 82, 79-91.

    4. Carrion, G., Huaman, J.L., Silva, M., Ampuero, J.S., Paz, I., Ocana, V.R., LagunaTorres, V.A., Hontz, R.D., 2016. Molecular epidemiology of coxsackievirus A16 strains from four sentinel surveillance sites in Peru. Int. J. Infect. Dis. 52, 83-85.

    5. Chen, J.F., Zhang, R.S., Ou, X.H., Chen, F.M., Sun, B.C., 2014. The role of enterovirus 71 and coxsackievirus A strains in a large outbreak of hand, foot, and mouth disease in 2012 in Changsha, China. Int. J. Infect. Dis. 28, 17-25.

    6. Chen, M., He, S., Yan, Q., Xu, X., Wu, W., Ge, S., Zhang, S., Chen, M., Xia, N., 2017. Severe hand, foot and mouth disease associated with Coxsackievirus A10 infections in Xiamen, China in 2015. J. Clin. Virol. 93, 20-24.

    7. Chen, X., Tan, X., Li, J., Jin, Y., Gong, L., Hong, M., Shi, Y., Zhu, S., Zhang, B., Zhang, S., Zhang, Y., Mao, N., Xu, W., 2013. Molecular epidemiology of coxsackievirus A16:intratype and prevalent intertype recombination identified. PLoS One 8, e82861.

    8. Dalldorf, G., 1953. The coxsackie virus group. Ann. N. Y. Acad. Sci. 56, 583-586.

    9. Davia, J.L., Bel, P.H., Ninet, V.Z., Bracho, M.A., Gonzalez-Candelas, F., Salazar, A., Gobernado, M., Bosch, I.F., 2011. Onychomadesis outbreak in Valencia, Spain associated with hand, foot, and mouth disease caused by enteroviruses. Pediatr. Dermatol. 28, 1-5.

    10. Fu, X., Wan, Z., Li, Y., Hu, Y., Jin, X., Zhang, C., 2020. National epidemiology and evolutionary history of four hand, foot and mouth disease-related enteroviruses in China from 2008 to 2016. Virol. Sin. 35, 21-33.

    11. Fu, Y., Sun, Q., Liu, B., Xu, H., Wang, Y., Zhu, W., Pan, L., Zhu, L., 2016. Epidemiological characteristics and pathogens attributable to hand, foot, and mouth disease in Shanghai, 2008-2013. J. Infect Dev. Ctries. 10, 612-618.

    12. Fuschino, M.E., Lamson, D.M., Rush, K., Carbone, L.S., Taff, M.L., Hua, Z., Landi, K., George, K.S., 2012. Detection of coxsackievirus A10 in multiple tissues of a fatal infant sepsis case. J. Clin. Virol. 53, 259-261.

    13. Ge, Y., Zheng, Y., Pan, H., Mao, S., Li, Y., Xia, A., Zhu, Q., Hu, J., Zeng, M., 2015.[Epidemiological surveillance of hand, foot and mouth disease in Shanghai, 2010-2014]. Zhonghua Er Ke Za Zhi 53, 676-683.

    14. Gibbs, M.J., Armstrong, J.S., Gibbs, A.J., 2000. Sister-scanning:a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16, 573-582.

    15. Guan, H., Wang, J., Wang, C., Yang, M., Liu, L., Yang, G., Ma, X., 2015. Etiology of multiple non-EV71 and non-CVA16 enteroviruses associated with hand, foot and mouth disease in Jinan, China, 2009-June 2013. PLoS One 10, e0142733.

    16. Hassel, C., Mirand, A., Farkas, A., Diedrich, S., Huemer, H.P., Peigue-Lafeuille, H., Archimbaud, C., Henquell, C., Bailly, J.L., Network, H.F.S., 2017. Phylogeography of coxsackievirus A16 reveals global transmission pathways and recent emergence and spread of a recombinant genogroup. J. Virol. 91, e00630-17.

    17. He, Y.Q., Chen, L., Xu, W.B., Yang, H., Wang, H.Z., Zong, W.P., Xian, H.X., Chen, H.L., Yao, X.J., Hu, Z.L., Luo, M., Zhang, H.L., Ma, H.W., Cheng, J.Q., Feng, Q.J., Zhao, D.J., 2013. 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. J. Clin. Microbiol. 51, 3560-3566.

    18. Hu, Y.F., Yang, F., Du, J., Dong, J., Zhang, T., Wu, Z.Q., 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.

    19. Ji, H., Fan, H., Lu, P.X., Zhang, X.F., Ai, J., Shi, C., Huo, X., Bao, C.J., Shan, J., Jin, Y., 2019. Surveillance for severe hand, foot, and mouth disease from 2009 to 2015 in Jiangsu province:epidemiology, etiology, and disease burden. BMC Infect. Dis. 19, 79.

    20. Ji, T., Guo, Y., Huang, W., Shi, Y., Xu, Y., Tong, W., Yao, W., Tan, Z., Zeng, H., Ma, J., Zhao, H., Han, T., Zhang, Y., Yan, D., Yang, Q., Zhu, S., Zhang, Y., Xu, W., 2018. The emerging sub-genotype C2 of CoxsackievirusA10 associated with hand, foot and mouth disease extensively circulating in mainland of China. Sci. Rep. 8, 13357.

    21. Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.

    22. Lam, H.M., Ratmann, O., Boni, M.F., 2018. Improved algorithmic complexity for the 3SEQ recombination detection algorithm. Mol. Biol. Evol. 35, 247-251.

    23. Li, J., Wang, X., Cai, J., Ge, Y., Wang, C., Qiu, Y., Xia, A., Zeng, M., 2020. Non-polio enterovirus infections in children with central nervous system disorders in Shanghai, 2016-2018:serotypes and clinical characteristics. J. Clin. Virol. 129, 104516.

    24. Li, Y., Bao, H., Zhang, X., Zhai, M., Bao, X., Wang, D., Zhang, S., 2017. Epidemiological and genetic analysis concerning the non-enterovirus 71 and non-coxsackievirus A16 causative agents related to hand, foot and mouth disease in Anyang city, Henan Province, China, from 2011 to 2015. J. Med. Virol. 89, 1749-1758.

    25. Li, Y., Chang, Z., Wu, P., Liao, Q., Liu, F., Zheng, Y., Luo, L., Zhou, Y., Chen, Q., Yu, S., Guo, C., Chen, Z., Long, L., Zhao, S., Yang, B., Yu, H., Cowling, B.J., 2018. Emerging enteroviruses causing hand, foot and mouth disease, China, 2010-2016. Emerg. Infect. Dis. 24, 1902-1906.

    26. Liu, S.L., Pan, H., Liu, P., Amer, S., Chan, T.C., Zhan, J., Huo, X., Liu, Y., Teng, Z., Wang, L., Zhuang, H., 2015. Comparative epidemiology and virology of fatal and nonfatal cases of hand, foot and mouth disease in mainland China from 2008 to 2014. Rev. Med. Virol. 25, 115-128.

    27. Liu, W., Wu, S., Xiong, Y., Li, T., Wen, Z., Yan, M., Qin, K., Liu, Y., Wu, J., 2014. Cocirculation and genomic recombination of coxsackievirus A16 and enterovirus 71 during a large outbreak of hand, foot, and mouth disease in Central China. PLoS One 9, e96051.

    28. Lu, Q.B., Zhang, X.A., Wo, Y., Xu, H.M., Li, X.J., Wang, X.J., Ding, S.J., Chen, X.D., He, C., Liu, L.J., Li, H., Yang, H., Li, T.Y., Liu, W., Cao, W.C., 2012. Circulation of Coxsackievirus A10 and A6 in hand-foot-mouth disease in China, 2009-2011. PLoS One 7, e52073.

    29. Lukashev, A.N., Shumilina, E.Y., Belalov, I.S., Ivanova, O.E., Eremeeva, T.P., Reznik, V.I., Trotsenko, O.E., Drexler, J.F., Drosten, C., 2014. Recombination strategies and evolutionary dynamics of the Human enterovirus A global gene pool. J. Gen. Virol. 95, 868-873.

    30. Martin, D., Rybicki, E., 2000. RDP:detection of recombination amongst aligned sequences. Bioinformatics 16, 562-563.

    31. Martin, D.P., Murrell, B., Golden, M., Khoosal, A., Muhire, B., 2015. RDP4:detection and analysis of recombination patterns in virus genomes. Virus Evol. 1, vev003.

    32. Martin, D.P., Posada, D., Crandall, K.A., Williamson, C., 2005. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res. Hum. Retrovir. 21, 98-102.

    33. Meng, X.D., Tong, Y., Wei, Z.N., Wang, L., Mai, J.Y., Wu, Y., Luo, Z.Y., Li, S., Li, M., Wang, S., Wei, S., Gong, W., Zhang, W., Hu, X., Huang, J., Shi, J., Yang, G., Meng, S., Wang, Z., Guan, X., Shen, S., 2020. Epidemical and etiological study on hand, foot and mouth disease following EV-A71 vaccination in Xiangyang, China. Sci. Rep. 10, 20909.

    34. Mirand, A., Henquell, C., Archimbaud, C., Ughetto, S., Antona, D., Bailly, J.L., PeigueLafeuille, H., 2012. 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.

    35. Munivenkatappa, A., Yadav, P.D., Nyayanit, D.A., Majumdar, T.D., Sangal, L., Jain, S., Sinha, D.P., Shrivastava, A., Mourya, D.T., 2018. Molecular diversity of Coxsackievirus A10 circulating in the southern and northern region of India[2009-17]. Infect. Genet. Evol. 66, 101-110.

    36. Oberste, M.S., Maher, K., Kilpatrick, D.R., Pallansch, M.A., 1999. Molecular evolution of the human enteroviruses:correlation of serotype with VP1 sequence and application to picornavirus classification. J. Virol. 73, 1941-1948.

    37. Oberste, M.S., Penaranda, S., Maher, K., Pallansch, M.A., 2004. Complete genome sequences of all members of the species Human enterovirus A. J. Gen. Virol. 85, 1597-1607.

    38. Okada, H., Wada, M., Sato, H., Yamaguchi, Y., Tanji, H., Kurokawa, K., Kawanami, T., Takahashi, T., Kato, T., 2013. Neuromyelitis optica preceded by hyperCKemia and a possible association with coxsackie virus group A10 infection. Intern. Med. 52, 2665-2668.

    39. Posada, D., Crandall, K.A., 2001. Evaluation of methods for detecting recombination from DNA sequences:computer simulations. Proc. Natl. Acad. Sci. U. S. A. 98, 13757-13762.

    40. Roth, B., Enders, M., Arents, A., Pfitzner, A., Terletskaia-Ladwig, E., 2007. Epidemiologic aspects and laboratory features of enterovirus infections in Western Germany, 2000-2005. J. Med. Virol. 79, 956-962.

    41. Saitou, N., Nei, M., 1987. The neighbor-joining method:a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.

    42. Smith, J.M., 1992. Analyzing the mosaic structure of genes. J. Mol. Evol. 34, 126-129.

    43. Song, C., Li, Y., Zhou, Y., Liang, L., Turtle, L., Wang, F., Wu, P., Qiu, Q., Yang, J., Wang, K., Cui, P., Cheng, Y., Zhang, T., Guo, C., Zeng, M., Long, L., Peiris, M., Zhou, C., Cowling, B.J., Yu, H., 2020. Enterovirus genomic load and disease severity among children hospitalised with hand, foot and mouth disease. EBioMedicine 62, 103078.

    44. Tan, X., Huang, X., Zhu, S., Chen, H., Yu, Q., Wang, H., Huo, X., Zhou, J., Wu, Y., Yan, D., Zhang, Y., Wang, D., Cui, A., An, H., Xu, W., 2011. The persistent circulation of enterovirus 71 in People's Republic of China:causing emerging nationwide epidemics since 2008. PLoS One 6, e25662.

    45. Tian, H., Zhang, Y., Shi, Y., Li, X., Sun, Q., Liu, L., Zhao, D., Xu, B., 2017. Epidemiological and aetiological characteristics of hand, foot, and mouth disease in Shijiazhuang City, Hebei province, China, 2009-2012. PLoS One 12, e0176604.

    46. Tian, H., Zhang, Y., Sun, Q., Zhu, S., Li, X., Pan, Z., Xu, W., Xu, B., 2014. 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 9, e84233.

    47. Wang, J., Teng, Z., Cui, X., Li, C., Pan, H., Zheng, Y., Mao, S., Yang, Y., Wu, L., Guo, X., Zhang, X., Zhu, Y., 2018. Epidemiological and serological surveillance of hand-footand-mouth disease in Shanghai, China, 2012-2016. Emerg. Microb. Infect. 7, 8.

    48. Weiller, G.F., 1998. Phylogenetic profiles:a graphical method for detecting genetic recombinations in homologous sequences. Mol. Biol. Evol. 15, 326-335.

    49. Xie, J., Yang, X.H., Hu, S.Q., Zhan, W.L., Zhang, C.B., Liu, H., Zhao, H.Y., Chai, H.Y., Chen, K.Y., Du, Q.Y., Liu, P., Yin, A.H., Luo, M.Y., 2020. Co-circulation of coxsackieviruses A-6, A-10, and A-16 causes hand, foot, and mouth disease in Guangzhou city, China. BMC Infect. Dis. 20, 271.

    50. Xing, W., Liao, Q., Viboud, C., Zhang, J., Sun, J., Wu, J.T., Chang, Z., Liu, F., Fang, V.J., Zheng, Y., Cowling, B.J., Varma, J.K., Farrar, J.J., Leung, G.M., Yu, H., 2014. Hand, foot, and mouth disease in China, 2008-12:an epidemiological study. Lancet Infect. Dis. 14, 308-318.

    51. Xu, M., Su, L., Cao, L., Zhong, H., Dong, N., Dong, Z., Xu, J., 2015. Genotypes of the enterovirus causing hand foot and mouth disease in Shanghai, China, 2012-2013. PLoS One 10, e0138514.

    52. Xu, M., Su, L., Cao, L., Zhong, H., Dong, N., Xu, J., 2013. Enterovirus genotypes causing hand foot and mouth disease in Shanghai, China:a molecular epidemiological analysis. BMC Infect. Dis. 13, 489.

    53. Yang, B., Liu, F., Liao, Q., Wu, P., Chang, Z., Huang, J., Long, L., Luo, L., Li, Y., Leung, G.M., Cowling, B.J., Yu, H., 2017. Epidemiology of hand, foot and mouth disease in China, 2008 to 2015 prior to the introduction of EV-A71 vaccine. Euro Surveill. 22, 16-00824.

    54. Yang, F., Zhang, T., Hu, Y., Wang, X., Du, J., Li, Y., Sun, S., Sun, X., Li, Z., Jin, Q., 2011. Survey of enterovirus infections from hand, foot and mouth disease outbreak in China, 2009. Virol. J. 8, 508.

    55. Zeng, M., Pu, D., Mo, X., Zhu, C., Gong, S., Xu, Y., Lin, G., Wu, B., He, S., Jiao, X., Wang, X., Wang, X., Zhu, Q., Altmeyer, R., 2013. Children of rural-to-urban migrant workers in China are at a higher risk of contracting severe hand, foot and mouth disease and EV71 infection:a hospital-based study. Emerg. Microb. Infect. 2, e72.

    56. Zhang, C., Zhu, R., Yang, Y., Chi, Y., Yin, J., Tang, X., Yu, L., Zhang, C., Huang, Z., Zhou, D., 2015. Phylogenetic analysis of the major causative agents of hand, foot and mouth disease in Suzhou City, Jiangsu province, China, in 2012-2013. Emerg. Microb. Infect. 4, e12.

    57. Zhang, J., Litvinova, M., Liang, Y., Zheng, W., Shi, H., Vespignani, A., Viboud, C., Ajelli, M., Yu, H., 2021. The impact of relaxing interventions on human contact patterns and SARS-CoV-2 transmission in China. Sci. Adv. 7, eabe2584.

    58. Zhang, Y., Tan, X., Cui, A., Mao, N., Xu, S., Zhu, Z., Zhou, J., Shi, J., Zhao, Y., Wang, X., Huang, X., Zhu, S., Zhang, Y., Tang, W., Ling, H., Xu, W., 2013. Complete genome analysis of the C4 subgenotype strains of enterovirus 71:predominant recombination C4 viruses persistently circulating in China for 14 years. PLoS One 8, e56341.

    59. Zhao, T.S., Du, J., Li, H.J., Cui, Y., Liu, Y., Yang, Y., Cui, F., Lu, Q.B., 2020. Molecular epidemiology and clinical characteristics of herpangina children in Beijing, China:a surveillance study. PeerJ 8, e9991.

    60. Zhuang, Z.C., Kou, Z.Q., Bai, Y.J., Cong, X., Wang, L.H., Li, C., Zhao, L., Yu, X.J., Wang, Z.Y., Wen, H.L., 2015. Epidemiological research on hand, foot, and mouth disease in mainland China. Viruses 7, 6400-6411.

  • 加载中

Article Metrics

Article views(5139) PDF downloads(21) Cited by()

Related
Proportional views

    Genomic surveillance of coxsackievirus A10 reveals genetic features and recent appearance of genogroup D in Shanghai, China, 2016-2020

      Corresponding author: Wanju Zhang, zhangwanju@scdc.sh.cn
      Corresponding author: Xi Zhang, zhangxi@scdc.sh.cn
      Corresponding author: Zheng Teng, tengzheng@scdc.sh.cn
    • a Microbiology Department, Shanghai Municipal Center for Disease Control and Prevention, Shanghai, 200336, China
    • b Microbiology Department, Songjiang District Center for Disease Control and Prevention, Shanghai, 201620, China
    • c WHO WPRO Regional Polio Reference Laboratory, NHC Key Laboratory for Biosafety, NHC Key Laboratory for Medical Virology, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, 102206, China

    Abstract: Coxsackievirus A10 (CVA10) is one of the major causative agents of hand, foot and mouth disease (HFMD). To investigate the epidemiological characteristics as well as genetic features of CVA10 currently circulating in Shanghai, China, we collected a total of 9,952 sporadic HFMD cases from January 2016 to December 2020. In the past five years, CVA10 was the fourth prevalent causatives associated with HFMD in Shanghai and the overall positive rate was 2.78%. The annual distribution experienced significant fluctuations over the past five years. In addition to entire VP1 sequencing, complete genome sequencing and recombination analysis of CVA10 isolates in Shanghai were further performed. A total of 64 near complete genomes and 11 entire VP1 sequences in this study combined with reference sequences publicly available were integrated into phylogenetic analysis. The CVA10 sequences in this study mainly belonged to genogroup C and presented 91%-100% nucleotide identity with other Chinese isolates based on VP1 region. For the first time, our study reported the appearance of CVA10 genogroup D in Chinese mainland, which had led to large-scale outbreaks in Europe previously. The recombination analysis showed the recombination break point located between 5,100 nt and 6,700 nt, which suggesting intertypic recombination with CVA16 genogroup D. To conclusion, CVA10 genogroup C was the predominant genogroup in Shanghai during 2016-2020. CVA10 recombinant genogroup D was firstly reported in circulating in Chinese mainland. Continuous surveillance is needed to better understand the evolution relationships and transmission pathways of CVA10 to help to guide disease control and prevention.

    Reference (60)

    目录

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return