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Molecular epidemiology of enterovirus from children with herpangina or hand, foot, and mouth disease in Hangzhou, 2016

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Abstract

Enteroviruses (EVs) are the major cause of hand, foot, and mouth disease (HFMD) and herpangina in children. In this study, we conducted a molecular investigation of EVs in throat swab samples from children in Hangzhou, China with a diagnosis of HFMD or herpangina. EVs were detected using one-step real-time RT-PCR, and their serotypes were determined based on partial VP1 gene sequences. The molecular typing results revealed the presence of six different EV serotypes in HFMD cases, including coxsackievirus (CV) A16 (20/30, 66.7%), CVA4 (3/30, 10.0%), CVA6 (3/30, 10.0%), EVA71 (2/30, 6.7%), CVB4 (1/30, 3.3%), and CVB5 (1/30, 3.3%). Eleven different EV serotypes were detected in herpangina cases, among which CVA4 was the most frequently detected serotype (105/170, 61.8%), followed by CVA16 (30/170, 17.6%), CVB4 (9/170, 5.3%), CVA6 (6/170, 3.5%), CVB3 (5/170, 2.9%), CVA10 (3/170, 1.8%), EVA71 (4/170, 2.4%), Echo9 (3/170, 1.8%), CVA9 (2/170, 1.2%), CVB1 (3/170, 1.8%) and CVA5 (1/170, 0.6%). The nucleotide sequence identity of EV strains from the same subtype ranged from 80.7% to 100%, and most of the EVs were closely related to virus strains found in Australia and mainland China. In conclusion, CVA 16 and CVA 4 were the main serotypes causing HFMD and herpangina, respectively, in children in Hangzhou in 2016. Most of these EVs were closely related to virus strains from Australia and mainland China.

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References

  1. Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, Lindberg AM, Pallansch MA, Palmenberg AC, Reuter G, Simmonds P, Skern T, Stanway G, Yamashita T, Ictv Report Consortium (2017) ICTV virus taxonomy profile: Picornaviridae. J Gen Virol 98(10):2421–2422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Nikolaidis M, Mimouli K, Kyriakopoulou Z, Tsimpidis M, Tsakogiannis D, Markoulatos P, Amoutzias GD (2019) Large-scale genomic analysis reveals recurrent patterns of intertypic recombination in human enteroviruses. Virology 526:72–80

    Article  CAS  PubMed  Google Scholar 

  3. Li W, Zhang X, Chen X, Cheng YP, Wu YD, Shu Q, Chen XJ, Shang SQ (2015) Epidemiology of childhood enterovirus infections in Hangzhou, China. Virol J 12:58

    Article  PubMed  PubMed Central  Google Scholar 

  4. Kim B, Moon S, Bae GR, Lee H, Pai H, Oh SH (2018) Factors associated with severe neurologic complications in patients with either hand-foot-mouth disease or herpangina: a nationwide observational study in South Korea, 2009–2014. PLoS One 13:e0201726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Wei L, Qiong Z, Xiao-Ting S, Yu-Jie L, Jian-Hua M, Qiang S, Shi-Qiang S (2016) Molecular epidemiological study of enteroviruses associated with encephalitis in children from Hangzhou, China. Med (Baltim) 95:e4870

    Article  Google Scholar 

  6. Li XW, Ni X, Qian SY, Wang Q, Jiang RM, Xu WB, Zhang YC, Yu GJ, Chen Q, Shang YX, Zhao CS, Yu H, Zhang T, Liu G, Deng HL, Gao J, Ran XG, Yang QZ, Xu BL, Huang XY, Wu XD, Bao YX, Chen YP, Chen ZH, Liu QQ, Lu GP, Liu CF, Wang RB, Zhang GL, Gu F, Xu HM, Li Y, Yang T (2018) Chinese guidelines for the diagnosis and treatment of hand, foot and mouth disease (2018 edition). World J Pediatr 14:437–447

    Article  PubMed  Google Scholar 

  7. Zhuang ZC, Kou ZQ, Bai YJ, Cong X, Wang LH, Li C, Zhao L, Yu XJ, Wang ZY, Wen HL (2015) Epidemiological research on hand, foot, and mouth disease in Mainland China. Viruses 7:6400–6411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zhao Y, Zhang H, Liu H, Zhang J, He L, Sun H, Huang X, Yang Z, Ma S (2018) Molecular characteristics of hand, foot, and mouth disease for hospitalized pediatric patients in Yunnan, China. Med (Baltim) 97:e11610

    Article  CAS  Google Scholar 

  10. Park K, Lee B, Baek K, Cheon D, Yeo S, Park J, Soh J, Cheon H, Yoon K, Choi Y (2012) Enteroviruses isolated from herpangina and hand-foot-and-mouth disease in Korean children. Virol J 9:205

    Article  PubMed  PubMed Central  Google Scholar 

  11. Lee MH, Huang LM, Wong WW, Wu TZ, Chiu TF, Chang LY (2011) Molecular diagnosis and clinical presentations of enteroviral infections in Taipei during the 2008 epidemic. J Microbiol Immunol Infect 44:178–183

    Article  PubMed  Google Scholar 

  12. Mirand A, Henquell C, Archimbaud C, Ughetto S, Antona D, Bailly JL, Peigue-Lafeuille 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:E110–118

    Article  CAS  PubMed  Google Scholar 

  13. Puenpa J, Mauleekoonphairoj J, Linsuwanon P, Suwannakarn K, Chieochansin T, Korkong S, Theamboonlers A, Poovorawan Y (2014) Prevalence and characterization of enterovirus infections among pediatric patients with hand foot mouth disease, herpangina and influenza like illness in Tailand, 2012. PLoS One 9(6):e98888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Oliveira DB, Campos RK, Soares MS, Barros RB, Batista TC, Ferreira PC, Bonjardim CA, Trindade GS, Abrahão JS, Kroon EG (2014) Outbreak of herpangina in the Brazilian Amazon in 2009 caused by Enterovirus B. Arch Virol 159:1155–1157

    Article  CAS  PubMed  Google Scholar 

  15. Yao X, Bian LL, Lu WW, Li JX, Mao QY, Wang YP, Gao F, Wu X, Ye Q, Li XL, Zhu FC, Liang Z (2017) Epidemiological and etiological characteristics of herpangina and hand foot mouth diseases in Jiangsu, China, 2013–2014. Hum Vaccine Immunother 13(4):823–830

    Article  Google Scholar 

  16. Zhang L, Yan J, Ojcius DM, Lv H, Miao Z, Chen Y, Zhang Y, Yan J (2013) Novel and predominant pathogen responsible for the enterovirus-associated encephalitis in eastern China. PLoS One 8:e85023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  Google Scholar 

  18. Weng Y, Chen W, He W, Huang M, Zhu Y, Yan Y (2017) Serotyping and genetic characterization of hand, foot, and mouth disease (HFMD)-associated enteroviruses of no-EV71 and non-CVA16 circulating in Fujian, China, 2011–2015. Med Sci Monit 23:2508–2518

    Article  PubMed  PubMed Central  Google Scholar 

  19. Chen L, Yao XJ, Xu SJ, Yang H, Wu CL, Lu J, Xu WB, Zhang HL, Meng J, Zhang Y, He YQ, Zhang RL (2019) Molecular surveillance of coxsackievirus A16 reveals the emergence of a new clade in mainland China. Arch Virol 164(3):867–874

    Article  CAS  PubMed  Google Scholar 

  20. Gao F, Bian L, Hao X, Hu Y, Yao X, Sun S, Chen P, Yang C, Du R, Li J, Zhu F, Mao Q, Liang Z (2018) Seroepidemiology of coxsackievirus B5 in infants and children in Jiangsu province, China. Hum Vaccin Immunother 14(1):74–80

    Article  PubMed  Google Scholar 

  21. Chen M, Ju Y, Chen M, Xie Z, Zhou K, Tan Y, Mo J (2017) Epidemiological and genetic characteristics of EV71 in hand, foot, and mouth disease in Guangxi, southern China, from 2010 to 2015. PLoS One 12(12):e0188640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Xia Y, Shan J, Ji H, Zhang J, Yang H, Shen Q, Ya X, Tian R, Wang C, Liu C, Ni C, Liu H (2016) Study of the epidemiology and etiological characteristics of hand, foot, and mouth disease in Suzhou City, East China, 2011–2014. Arch Virol 161:1933–1943

    Article  CAS  PubMed  Google Scholar 

  23. He S, Chen M, Wu W, Yan Q, Zhuo Z, Su X, Zhang S, Ge S, Xia N (2018) An emerging and expanding clade accounts for the persistent outbreak of Coxsackievirus A6-associated hand, foot, and mouth disease in China since 2013. Virology 518:328–334

    Article  CAS  PubMed  Google Scholar 

  24. 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-foot-and-mouth disease in Shanghai, China, 2012–2016. Emerg Microbes Infect 7:8

    PubMed  PubMed Central  Google Scholar 

  25. Li W, Gao HH, Zhang Q, Liu YJ, Tao R, Cheng YP, Shu Q, Shang SQ (2016) Large outbreak of herpangina in children caused by enterovirus in summer of 2015 in Hangzhou, China. Sci Rep 6:35388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was funded by The Key Technologies R&D Program of the National Ministry of Science (2018ZX10734-401), the Medical Scientiic Projects from the Health Department of Zhejiang Province (2015KYA119) and the National Nature Science Foundation of China (81671495 and 81701535).

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Author notes

  1. Wei Li and Cixiu Li contributed equally to this work.

Authors and Affiliations

  1. Department of Clinical Laboratory, Children’s Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of China

    Wei Li, Lifang Liu & Shiqiang Shang

  2. Department of Microbiology Laboratory, Zhejiang Provincial Centre for Disease Control and Prevention, 3399 Binsheng Road, Hangzhou, People’s Republic of China

    Cixiu Li, Haiyan Mao & Yanjun Zhang

  3. School of Basic Medicine, Zhejiang University, Hangzhou, People’s Republic of China

    Cixiu Li

  4. Department of Clinical Laboratory, Affiliated Hospital of Hangzhou Normal University, Hangzhou, People’s Republic of China

    Xia Liu

Authors
  1. Wei Li
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  2. Cixiu Li
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  4. Xia Liu
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Correspondence to Haiyan Mao or Yanjun Zhang.

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This study was approved by the medical ethics committee of the Children’s Hospital of Zhejiang University School of Medicine.

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Li, W., Li, C., Liu, L. et al. Molecular epidemiology of enterovirus from children with herpangina or hand, foot, and mouth disease in Hangzhou, 2016. Arch Virol 164, 2565–2571 (2019). https://doi.org/10.1007/s00705-019-04356-0

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