{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T05:59:41Z","timestamp":1792216781103,"version":"4.4.0"},"reference-count":36,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,3,23]],"date-time":"2017-03-23T00:00:00Z","timestamp":1490227200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,3,23]],"date-time":"2017-03-23T00:00:00Z","timestamp":1490227200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>To understand control interventions, the molecular epidemiology of acute hemorrhagic conjunctivitis (AHC) was investigated from 2004 to 2014.A total of 613,485 AHC cases (annualized cases 55,771) with two deaths were included. Our findings showed that AHC was reported in all provinces, predominantly in Southern and Eastern China. The incidence rates were highest in 2007 (5.65\/100,000) and 2010 (21.78\/100,000) respectively. A clear seasonal pattern was identified with a peak from August to October. AHC cases occurred in all age groups; however, five to 14 years was the predominant group [23.06%, 133, 510\/578,909]. The median age was 24 years (one month~97 years). The median duration from onset to diagnosis was 1.5 days, and there was no difference between the &lt;15, 15~60 and &gt;60-year-old patients [<jats:italic>p<\/jats:italic>\u2009=\u20090.0653]. The phylogenetic analysis of 100 nonstructural proteins (3C) and 84 structural proteins (VP1) revealed that AHC outbreaks were caused by Coxsackievirus A24 variant. Genotypes G4-c5a, G4-c5b, and G4-c3 co-circulated with both temporal and geographical overlaps. In conclusion, despite the overall steady decline in the number of AHC cases since the peak in 2010, it still remains a serious public health problem in Southern and Eastern China that targets on the school aged children under 15 years old.<\/jats:p>","DOI":"10.1038\/srep45202","type":"journal-article","created":{"date-parts":[[2017,3,23]],"date-time":"2017-03-23T11:25:42Z","timestamp":1490268342000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":37,"title":["Molecular epidemiology of acute hemorrhagic conjunctivitis caused by coxsackie A type 24 variant in China, 2004\u20132014"],"prefix":"10.1038","volume":"7","author":[{"given":"Li","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Na","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaodan","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiuming","family":"Jin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xingyi","family":"Geng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ta-Chien","family":"Chan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shelan","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,3,23]]},"reference":[{"key":"BFsrep45202_CR1","first-page":"173","volume":"45","author":"PW Wright","year":"1992","unstructured":"Wright, P. W., Strauss, G. H. & Langford, M. P. Acute hemorrhagic conjunctivitis. Am Fam Physician 45, 173\u2013178 (1992).","journal-title":"Am Fam Physician"},{"key":"BFsrep45202_CR2","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1002\/jmv.20304","volume":"75","author":"P Dussart","year":"2005","unstructured":"Dussart, P. et al. Outbreak of acute hemorrhagic conjunctivitis in French Guiana and West Indies caused by coxsackievirus A24 variant: phylogenetic analysis reveals Asian import. J Med Virol 75, 559\u2013565, doi: 10.1002\/jmv.20304 (2005).","journal-title":"J Med Virol"},{"key":"BFsrep45202_CR3","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1016\/j.jcv.","volume":"45","author":"PY Chu","year":"2009","unstructured":"Chu, P. Y. et al. Molecular epidemiology of coxsackie A type 24 variant in Taiwan, 2000\u20132007. J Clin Virol 45, 285\u2013291, doi: 10.1016\/j.jcv. (2009).","journal-title":"J Clin Virol"},{"key":"BFsrep45202_CR4","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1038\/eye.2009.","volume":"24","author":"PC Kuo","year":"2010","unstructured":"Kuo, P. C. et al. Molecular and immunocytochemical identification of coxsackievirus A-24 variant from the acute haemorrhagic conjunctivitis outbreak in Taiwan in 2007. Eye (Lond) 24, 131\u2013136, doi: 10.1038\/eye.2009. (2010).","journal-title":"Eye (Lond)"},{"key":"BFsrep45202_CR5","doi-asserted-by":"publisher","first-page":"e23206","DOI":"10.1371\/journal.pone.","volume":"6","author":"FN Tavares","year":"2011","unstructured":"Tavares, F. N. et al. Molecular characterization and phylogenetic study of coxsackievirus A24v causing outbreaks of acute hemorrhagic conjunctivitis (AHC) in Brazil. PLoS One 6, e23206, doi: 10.1371\/journal.pone. (2011).","journal-title":"PLoS One"},{"key":"BFsrep45202_CR6","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.jviromet.","volume":"159","author":"XL Xiao","year":"2009","unstructured":"Xiao, X. L. et al. Simultaneous detection of enterovirus 70 and coxsackievirus A24 variant by multiplex real-time RT-PCR using an internal control. J Virol Methods 159, 23\u201328, doi: 10.1016\/j.jviromet. (2009).","journal-title":"J Virol Methods"},{"key":"BFsrep45202_CR7","unstructured":"Centers for Disease, C. & Prevention. Acute hemorrhagic conjunctivitis outbreak caused by Coxsackievirus A24\u2013Puerto Rico, 2003. MMWR Morb Mortal Wkly Rep 53, 632\u2013634 (2004)."},{"key":"BFsrep45202_CR8","first-page":"248","volume":"57","author":"P Thongcharoen","year":"1974","unstructured":"Thongcharoen, P., Jatikavanij, V., Wasi, C., Panatana, P. & Dumavibhat, P. An outbreak of acute hemorrhagic conjunctivitis in Thailand. 2. Epidemiologic investigation. J Med Assoc Thai 57, 248\u2013251 (1974).","journal-title":"J Med Assoc Thai"},{"key":"BFsrep45202_CR9","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/0002-9394(83)90332-X","volume":"95","author":"VE Sklar","year":"1983","unstructured":"Sklar, V. E. et al. Clinical findings and results of treatment in an outbreak of acute hemorrhagic conjunctivitis in southern Florida. Am J Ophthalmol 95, 45\u201354 (1983).","journal-title":"Am J Ophthalmol"},{"key":"BFsrep45202_CR10","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1007\/s00705-012-1520-7","volume":"158","author":"D Shukla","year":"2013","unstructured":"Shukla, D., Kumar, A., Srivastava, S. & Dhole, T. N. Molecular identification and phylogenetic study of coxsackievirus A24 variant isolated from an outbreak of acute hemorrhagic conjunctivitis in India in 2010. Arch Virol 158, 679\u2013684, doi: 10.1007\/s00705-012-1520-7 (2013).","journal-title":"Arch Virol"},{"key":"BFsrep45202_CR11","doi-asserted-by":"publisher","first-page":"1283","DOI":"10.1001\/jama.1983.03330340025025","volume":"249","author":"PA Patriarca","year":"1983","unstructured":"Patriarca, P. A. et al. Acute hemorrhagic conjunctivitis Investigation of a large-scale community outbreak in Dade County, Florida. JAMA 249, 1283\u20131289 (1983).","journal-title":"JAMA"},{"key":"BFsrep45202_CR12","doi-asserted-by":"publisher","first-page":"1010","DOI":"10.3201\/eid0908.030190","volume":"9","author":"MD Oh","year":"2003","unstructured":"Oh, M. D. et al. Acute hemorrhagic conjunctivitis caused by coxsackievirus A24 variant, South Korea, 2002. Emerg Infect Dis 9, 1010\u20131012, doi: 10.3201\/eid0908.030190 (2003).","journal-title":"Emerg Infect Dis"},{"key":"BFsrep45202_CR13","doi-asserted-by":"publisher","first-page":"e86883","DOI":"10.1371\/journal.pone.0086883","volume":"9","author":"B Wu","year":"2014","unstructured":"Wu, B. et al. Genetic characteristics of the coxsackievirus A24 variant causing outbreaks of acute hemorrhagic conjunctivitis in Jiangsu, China, 2010. PLoS One 9, e86883, doi: 10.1371\/journal.pone.0086883 (2014).","journal-title":"PLoS One"},{"key":"BFsrep45202_CR14","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1186\/1743-422X-10-96","volume":"10","author":"EA Ayoub","year":"2013","unstructured":"Ayoub, E. A. et al. A molecular investigative approach to an outbreak of acute hemorrhagic conjunctivitis in Egypt, October 2010. Virol J 10, 96, doi: 10.1186\/1743-422X-10-96 (2013).","journal-title":"Virol J"},{"key":"BFsrep45202_CR15","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1016\/j.virusres.2008.06.011","volume":"137","author":"A Khan","year":"2008","unstructured":"Khan, A., Sharif, S., Shaukat, S., Khan, S. & Zaidi, S. An outbreak of acute hemorrhagic conjunctivitis (AHC) caused by coxsackievirus A24 variant in Pakistan. Virus Res 137, 150\u2013152, doi: 10.1016\/j.virusres.2008.06.011 (2008).","journal-title":"Virus Res"},{"key":"BFsrep45202_CR16","first-page":"1","volume":"8","author":"WK Chang","year":"1977","unstructured":"Chang, W. K., Liu, K. C., Foo, T. C., Lam, M. W. & Chan, C. F. Acute haemorrhagic conjunctivitis in Hong Kong 1971\u20131975. Southeast Asian J Trop Med Public Health 8, 1\u20136 (1977).","journal-title":"Southeast Asian J Trop Med Public Health"},{"key":"BFsrep45202_CR17","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1186\/1743-422X-9-41","volume":"9","author":"W De","year":"2012","unstructured":"De, W. et al. Phylogenetic and molecular characterization of coxsackievirus A24 variant isolates from a 2010 acute hemorrhagic conjunctivitis outbreak in Guangdong, China. Virol J 9, 41, doi: 10.1186\/1743-422X-9-41 (2012).","journal-title":"Virol J"},{"key":"BFsrep45202_CR18","doi-asserted-by":"publisher","first-page":"1762","DOI":"10.1002\/jmv.21288","volume":"80","author":"D Wu","year":"2008","unstructured":"Wu, D. et al. Multiple outbreaks of acute hemorrhagic conjunctivitis due to a variant of coxsackievirus A24: Guangdong, China, 2007. J Med Virol 80, 1762\u20131768, doi: 10.1002\/jmv.21288 (2008).","journal-title":"J Med Virol"},{"key":"BFsrep45202_CR19","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1186\/1743-422X-7-138","volume":"7","author":"D Yan","year":"2010","unstructured":"Yan, D. et al. Outbreak of acute hemorrhagic conjunctivitis in Yunnan, People\u2019s Republic of China, 2007. Virol J 7, 138, doi: 10.1186\/1743-422X-7-138 (2010).","journal-title":"Virol J"},{"key":"BFsrep45202_CR20","unstructured":"Centers for Disease, C. Acute hemorrhagic conjunctivitis caused by coxsackievirus A24\u2013Caribbean. MMWR Morb Mortal Wkly Rep 36, 245\u2013246, 251 (1987)."},{"key":"BFsrep45202_CR21","first-page":"496","volume":"34","author":"H Li","year":"2013","unstructured":"Li, H. et al. Study on the complete sequence of CA24 variant isolated during the acute hemorrhagic conjunctivitis outbreaks in Zhejiang province during 2002 to 2010. Zhonghua Liu Xing Bing Xue Za Zhi 34, 496\u2013502 (2013).","journal-title":"Zhonghua Liu Xing Bing Xue Za Zhi"},{"key":"BFsrep45202_CR22","first-page":"421","volume":"27","author":"JY Yan","year":"2011","unstructured":"Yan, J. Y. et al. [Study on the pathological and molecular characteristics of AHC epidemic in Zhejiang Province in 2010]. Bing Du Xue Bao 27, 421\u2013426 (2011).","journal-title":"Bing Du Xue Bao"},{"key":"BFsrep45202_CR23","doi-asserted-by":"publisher","first-page":"1085","DOI":"10.2147\/OPTH.S81386","volume":"9","author":"K Harada","year":"2015","unstructured":"Harada, K., Fujimoto, T., Asato, Y. & Uchio, E. Virological and epidemiological analysis of coxsackievirus A24 variant epidemic of acute hemorrhagic conjunctivitis in Okinawa, Japan, in 2011. Clin Ophthalmol 9, 1085\u20131092, doi: 10.2147\/OPTH.S81386 (2015).","journal-title":"Clin Ophthalmol"},{"key":"BFsrep45202_CR24","first-page":"473","volume":"12","author":"KT Goh","year":"1981","unstructured":"Goh, K. T., Doraisingham, S. & Yin-Murphy, M. An epidemic of acute conjunctivitis caused by enterovirus-70 in Singapore in 1980. The Southeast Asian journal of tropical medicine and public health 12, 473\u2013486 (1981).","journal-title":"The Southeast Asian journal of tropical medicine and public health"},{"key":"BFsrep45202_CR25","first-page":"267","volume":"56","author":"P Dumavibhat","year":"1973","unstructured":"Dumavibhat, P. et al. An outbreak of acute hemorrhagic conjunctivitis in Thailand. I. Clinical observations. J Med Assoc Thai 56, 267\u2013272 (1973).","journal-title":"J Med Assoc Thai"},{"key":"BFsrep45202_CR26","first-page":"244","volume":"27","author":"P Kosrirukvongs","year":"1996","unstructured":"Kosrirukvongs, P., Kanyok, R., Sitritantikorn, S. & Wasi, C. Acute hemorrhagic conjunctivitis outbreak in Thailand, 1992. Southeast Asian J Trop Med Public Health 27, 244\u2013249 (1996).","journal-title":"Southeast Asian J Trop Med Public Health"},{"key":"BFsrep45202_CR27","doi-asserted-by":"publisher","first-page":"3087","DOI":"10.1017\/S0950268815000643","volume":"143","author":"J Chansaenroj","year":"2015","unstructured":"Chansaenroj, J. et al. Epidemic outbreak of acute haemorrhagic conjunctivitis caused by coxsackievirus A24 in Thailand, 2014. Epidemiol Infect 143, 3087\u20133093, doi: 10.1017\/S0950268815000643 (2015).","journal-title":"Epidemiol Infect"},{"key":"BFsrep45202_CR28","doi-asserted-by":"crossref","unstructured":"Marguerite, N. et al. A major outbreak of conjunctivitis caused by coxsackievirus A24, Reunion, January to April 2015. Euro Surveill 21, doi: 10.2807\/1560-7917.ES.2016.21.26.30271 (2016).","DOI":"10.2807\/1560-7917.ES.2016.21.26.30271"},{"key":"BFsrep45202_CR29","doi-asserted-by":"publisher","first-page":"2005","DOI":"10.1007\/s00705-007-1032-z","volume":"152","author":"DS Yeo","year":"2007","unstructured":"Yeo, D. S. et al. Molecular identification of coxsackievirus A24 variant, isolated from an outbreak of acute hemorrhagic conjunctivitis in Singapore in 2005. Arch Virol 152, 2005\u20132016, doi: 10.1007\/s00705-007-1032-z (2007).","journal-title":"Arch Virol"},{"key":"BFsrep45202_CR30","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1002\/jmv.1046","volume":"64","author":"KH Lin","year":"2001","unstructured":"Lin, K. H. et al. Genetic analysis of recent Taiwanese isolates of a variant of coxsackievirus A24. J Med Virol 64, 269\u2013274 (2001).","journal-title":"J Med Virol"},{"key":"BFsrep45202_CR31","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1159\/000149850","volume":"4","author":"RR Mirkovic","year":"1974","unstructured":"Mirkovic, R. R., Schmidt, N. J., Yin-Murphy, M. & Melnick, J. L. Enterovirus etiology of the 1970 Singapore epidemic of acute conjunctivitis. Intervirology 4, 119\u2013127 (1974).","journal-title":"Intervirology"},{"key":"BFsrep45202_CR32","first-page":"192","volume":"25","author":"KH Lim","year":"1973","unstructured":"Lim, K. H. & Yin-Murphy, M. Epidemic conjunctivitis in Singapore in 1970 and 1971. Trans Ophthalmol Soc N Z 25, 192\u2013195 (1973).","journal-title":"Trans Ophthalmol Soc N Z"},{"key":"BFsrep45202_CR33","first-page":"86","volume":"14","author":"KH Lim","year":"1973","unstructured":"Lim, K. H. & Yin-Murphy, M. Epidemic conjunctivitis in Singapore in 1970 and 1971. Singapore Med J 14, 86\u201389 (1973).","journal-title":"Singapore Med J"},{"key":"BFsrep45202_CR34","first-page":"247","volume":"12","author":"KH Lim","year":"1971","unstructured":"Lim, K. H. & Yin-Murphy, M. An epidemic of conjunctivitis in Singapore in 1970. Singapore Med J 12, 247\u2013249 (1971).","journal-title":"Singapore Med J"},{"key":"BFsrep45202_CR35","doi-asserted-by":"publisher","first-page":"748","DOI":"10.1016\/0042-6822(92)90477-7","volume":"187","author":"H Ishiko","year":"1992","unstructured":"Ishiko, H. et al. Phylogenetic analysis of a coxsackievirus A24 variant: the most recent worldwide pandemic was caused by progenies of a virus prevalent around 1981. Virology 187, 748\u2013759 (1992).","journal-title":"Virology"},{"key":"BFsrep45202_CR36","doi-asserted-by":"publisher","first-page":"e0160672","DOI":"10.1371\/journal.pone.0160672","volume":"11","author":"YC Yen","year":"2016","unstructured":"Yen, Y. C. et al. Phylodynamic Characterization of an Ocular-Tropism Coxsackievirus A24 Variant. PLoS One 11, e0160672, doi: 10.1371\/journal.pone.0160672 (2016).","journal-title":"PLoS One"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep45202.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep45202","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep45202.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T23:49:44Z","timestamp":1671839384000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep45202"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,3,23]]},"references-count":36,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,5,30]]}},"alternative-id":["BFsrep45202"],"URL":"https:\/\/doi.org\/10.1038\/srep45202","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,3,23]]},"assertion":[{"value":"26 October 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 February 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 March 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"45202"}}