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      Genetic Characteristics of the Coxsackievirus A24 Variant Causing Outbreaks of Acute Hemorrhagic Conjunctivitis in Jiangsu, China, 2010

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          Abstract

          During September 2010, an outbreak of acute hemorrhagic conjunctivitis reemerged in Jiangsu, three years after the nationwide epidemic in China in 2007. In total, 2409 cases were reported, 2118 of which were reported in September; 79.8% of those affected were students or teachers, with a median age of 16 years. To identify and demonstrate the genetic characteristics of the etiological agent, 52 conjunctival swabs were randomly collected from four different cities. After detection and isolation, 43 patients were positive for coxsackievirus A24 variant according to PCR and 20 according to culture isolation. Neither adenovirus nor EV70 was detected. A phylogenetic study of the complete 3Cpro and VP1 regions showed that the Jiangsu isolates clustered into a new lineage, GIV-C5, with two uniform amino-acid mutations that distinguished them from all previous strains. Another new cluster, GIV-C4, formed by Indian isolates from 2007 and Brazilian isolates from 2009, was also identified in this study. Interestingly, our isolates shared greatest homology with the GIV-C4 strains, not with the isolates that were responsible for the nationwide acute hemorrhagic conjunctivitis epidemic in China in 2007. Although all our isolates were closely related, they could be differentiated into two subclusters within GIV-C5. In conclusion, our study suggests that a new cluster of coxsackievirus A24 variant that had already evolved into diverse strains was associated with the acute hemorrhagic conjunctivitis outbreaks in Jiangsu in September 2010. These viruses might have originated from the virus isolated in India in 2007, rather than from the epidemic strains isolated in China in 2007.

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          Acute Hemorrhagic Conjunctivitis caused by Coxsackievirus A24 Variant, South Korea, 2002

          In summer 2002, a nationwide outbreak of acute hemorrhagic conjunctivitis occurred in South Korea. The etiologic agent was confirmed as coxsackievirus A24 variant (CA24v) by virus isolation and sequencing of a part of the VP1 gene. Phylogentic analysis, based on the protease 3C sequences, showed that the Korean isolates were clustered into a lineage distinct from the CA24v isolates reported in previous outbreaks in Asia.
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            Outbreak of acute hemorrhagic conjunctivitis in Yunnan, People's Republic of China, 2007

            An outbreak of acute hemorrhagic conjunctivitis (AHC) occurred in Yunnan Province, China between August and September in 2007. A total of 3,597 cases were officially reported and the incidence rate reached 1390.94/100,000. Descriptive epidemiological analysis of the outbreak was conducted using the data from National Disease Supervision Information Management System (NDSIMS). To determine the causative agent for this outbreak and to analyze their genetic features, 30 conjunctival swabs and 19 paired serum specimens of acute and convalescent phase were collected from 30 patients with AHC, and viral isolation, molecular typing, antibody assay and phylogenetic analysis were performed. 11 virus strains were isolated from 30 conjunctival swabs. Amplification and sequencing of the VP4 region of these strains identified that coxsackievirus A24 variant (CA24v) could be the causative agent of the AHC outbreak and this was further confirmed by subsequent virus neutralizing antibody test on 19 paired serum specimens. Phylogenetic analysis based on the 3C regions showed that the Yunnan CA24v strains belonged to Group 3 and clustered with the strains isolated from worldwide AHC outbreaks after 2002. Phylogenetic analysis based on the partial VP1 revealed that the Yunnan strains differed from the strains isolated from AHC outbreak in Guangdong of China in 2007 with 2.8 - 3.0% nucleotide divergence, suggesting that two different lineages of CA24v caused the independent AHC outbreaks in Yunnan and Guangdong, respectively.
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              Multiple outbreaks of acute hemorrhagic conjunctivitis due to a variant of coxsackievirus A24: Guangdong, China, 2007.

              Acute hemorrhagic conjunctivitis (AHC) is usually caused by enterovirus 70, coxsackievirus A24(CA24v) and adenoviruses. Several outbreaks of AHC caused by a CA24v have occurred since it was imported into China in 1971. Multiple outbreaks of AHC reappeared in 10 cities of Guangdong during June to November in 2007. The epidemic began in the June, and spread extensively, with a peak in the September. A total of 31,659 cases were reported to center for disease control and prevention of Guangdong, it was estimated that the number of actual AHC was >200 thousands. Forty conjunctival swab specimens were collected from the cases diagnosed clinically with AHC. (RT)-PCR testing on these conjunctival specimens revealed the presence of an enterovirus, and this was confirmed by 16 isolates. We demonstrated the most likely etiological agent for the multiple outbreaks was a variant of coxsackievirus A24 by molecular typing using a partial VP1 sequence. Sequence comparison and phylogenetic analyses of the VP1 and 3Cpro gene regions were performed by Neighbor-joining method, the strains from different outbreaks and different geographical areas within Guangdong had no sequence divergence in 2007. The representative isolates from mainland of China including Hangzhou, Ningbo, Beijing, Yunnan, Liaoning, and Henan were analyzed in this study. Phylogenetic analysis revealed theses isolates were located in different clusters, a close phylogenetic and chronological relationship with Singaporean, South Korean and Thailand isolates had been observed. This confirms CA24v circulated in China's mainland has not evolved independently, but co-evolved with the isolates of Southeast Asia.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                24 January 2014
                : 9
                : 1
                : e86883
                Affiliations
                [1]Department of Acute Infectious Disease Control and Prevention, Jiangsu Province Center for Disease Control and Prevention, Nanjing, Jiangsu, China
                University of Texas Medical Branch, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: BW YZ MZ. Performed the experiments: BW XQ KX HJ. Analyzed the data: BW FT MZ. Contributed reagents/materials/analysis tools: XQ KX HJ FT MZ. Wrote the paper: BW YZ.

                Article
                PONE-D-13-38461
                10.1371/journal.pone.0086883
                3901726
                24475191
                37879e2a-cf1a-4908-9d64-45b541256c75
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 18 September 2013
                : 19 December 2013
                Page count
                Pages: 7
                Funding
                The study was supported by Jiangsu Province Health Development Project with Science and Education (ZX201109, RC2011084 and RC2011085). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Microbiology
                Virology
                Viral Classification
                RNA viruses
                Emerging Viral Diseases
                Viral Disease Diagnosis
                Viral Evolution
                Medicine
                Epidemiology
                Infectious Disease Epidemiology
                Molecular Epidemiology
                Infectious Diseases
                Viral Diseases
                Enterovirus Infection

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