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      Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013–2014

      brief-report
      a , b , World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization (WHO/OIE/FAO) H5 Evolution Working Group
      Influenza and Other Respiratory Viruses
      John Wiley & Sons, Ltd
      clade nomenclature, H5 subtype, hemagglutinin, highly pathogenic avian influenza, molecular epidemiology, phylogenetics, viral evolution

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          Abstract

          Aim

          The A/goose/Guangdong/1/96-like hemagglutinin (HA) genes of highly pathogenic avian influenza (HPAI) A(H5) viruses have continued to rapidly evolve since the most recent update to the H5 clade nomenclature by the WHO/OIE/FAO H5N1 Evolution Working Group. New clades diverging beyond established boundaries need to be identified and designated accordingly.

          Method

          Hemagglutinin sequences deposited in publicly accessible databases up to December 31, 2014, were analyzed by phylogenetic and average pairwise distance methods to identify new clades that merit nomenclature changes.

          Results

          Three new clade designations were recommended based on division of clade 2·1·3·2a (Indonesia), 2·2·1 (Egypt), and 2·3·4 (widespread detection in Asia, Europe, and North America) that includes newly emergent HPAI virus subtypes H5N2, H5N3, H5N5, H5N6, and H5N8.

          Conclusion

          Continued global surveillance for HPAI A(H5) viruses in all host species and timely reporting of sequence data will be critical to quickly identify new clades and assess their potential impact on human and animal health.

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          Most cited references24

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          Novel Reassortant Influenza A(H5N8) Viruses, South Korea, 2014

          To the Editor: Highly pathogenic avian influenza (HPAI) viruses have caused considerable economic losses to the poultry industry and poses potential threats to animal and human health (www.oie.int/en/ and www.who.int/en/). Since 2003, influenza A(H5N1) viruses with a hemagglutinin (HA) gene derived from A/goose/Guandong/1/96–like viruses have become endemic to 6 countries (Bangladesh, China, Egypt, India, Indonesia, and Vietnam) ( 1 ) (www.cdc.gov/). Furthermore, HPAI viruses with an H5 subtype continue to undergo substantial evolution because of extensive genetic divergence and reassortment between other subtypes of influenza viruses. Especially in China, novel subtypes of H5 HPAI virus, such as influenza A(H5N2), influenza A(H5N5), and influenza A(H5N8) viruses, were reported during 2009–2011 ( 2 , 3 ). On January 16, 2014, clinical signs of HPAI, such as decreased egg production (60%) and slightly increased mortality rates, were detected in ducks on a breeder duck farm near the Donglim Reservoir in Jeonbuk Province, South Korea. On January 17, a farmer (5 km from the Donglim Reservoir) also reported clinical signs of HPAI in breeder ducks. In addition, 100 carcasses of Baikal teals were found in the Donglim Reservoir. RNAs extracted from organs (liver, pancreas, and trachea) of 3 dead birds (1 breeder duck, 1 broiler duck, and 1 Baikal teal) were positive for H5 subtype virus by reverse transcription PCR ( 4 ). We isolated viruses from suspected specimens by inoculation into embryonated specific pathogen–free chicken eggs. The H5N8 subtype was identified by using HA and neuraminidase (NA) inhibition assays. Three viruses isolated from domestic ducks and wild birds were designated A/breeder duck/Korea/Gochang1/2014 (H5N8) (Gochang1), A/duck/Korea/Buan2/2014 (H5N8) (Buan2), and A/Baikal Teal/Korea/Donglim3/2014 (H5N8) (Donglim3). All 8 RNA genome segments of these viruses were amplified by using segment-specific primers and directly sequenced ( 5 ). Sequences of the 8 RNA segments of each virus were submitted to GenBank under accession nos. KJ413831–KJ413854. Gochang1 virus has been shown to be highly pathogenic for chickens (intravenous pathogenicity index 3.0) ( 6 ). This finding was consistent with analysis of the HA gene, as shown by a series of deduced basic amino acid sequences (Gochang1, LREKRRKR/GLF, Buan2 and Donglim3, LRERRRKR/GLF) at cleavage sites of HA ( 6 ). This outbreak of influenza A(H5N8) infection in South Korea was reported to the World Organisation for Animal Health ( 7 ). Nucleotide identity analysis with BioEdit version 7.2.5 (http://bioedit.software.informer.com/) and ClustalW (www.ebi.ac.kr/Tolls/clustalw2) showed that 3 distinct novel influenza A(H5N8) viruses emerged in South Korea. Gochang1 virus had 87%–97% sequence identities in the 8 genome segments with sequences for Buan2 and Donglim3 viruses, which had high sequence identities (>99.5%) with each other. Conservative amino acid residues within receptor binding pockets of HA (including E190, R220, G225, Q226, and G228; H3 numbering) were present in all 3 viruses, which indicated that these viruses retained affinity for the avian (sialic acid-2,3-NeuAcGal) cell surface ( 8 ). Although there was an I314V mutation in the NA of the 3 viruses, other mutations that encode oseltamivir and zanamivir resistance were not detected ( 9 ). A BLAST (www.ncbi.nlm.nih.gov/genomes/FLU/FLU.html) search and phylogenetic analysis showed that these novel H5N8 subtype viruses likely originated from reassortment between A/duck/Jiangsu/k1203/2010 (H5N8) virus and other subtypes of avian influenza virus, all of which co-circulated in birds in eastern China during 2009–2012 ( 10 ). A phylogenetic tree of partial HA gene sequences for the 3 virus isolates from South Korea and other H5 subtype viruses (n = 72), showed that Gochang1, Buan2, and Donglime3 belong to the proposed H5 clade 2.3.4.6 (Figure) ( 10 ). Figure Phylogenetic tree of hemagglutin (HA) genes of influenza A(H5N8) viruses, South Korea, 2014. Triangles indicate viruses characterized in this study. Other viruses detected in South Korea are indicated in boldface. Subtypes are indicated in parentheses. A total of 72 HA gene sequences were ≥1,600 nt. Multiple sequence alignment was performed by using ClustalW (www.ebi.ac.kr/Tolls/clustalw2). The tree was constructed by using the neighbor-joining method with the Kimura 2-parameter model and MEGA version 5.2 (www.megasoftware.net/) with 1,000 bootstrap replicates. H5, hemagglutinin 5; Gs/Gd, Goose/Guangdong; LPAI, low pathogenic avian influenza; HPAI, highly pathogenic avian influenza. Scale bar indicates nucleotide substitutions per site. The H5 and N8 genes of the 3 viruses had high nucleotide identities with A/duck/Jiangsu/k1203/2010 (H5N8) (JQ97369691–98) (H5: Gochang1, 98.9%, Buan2 and Donglim3, 97.2%; N8: Gochang1, 98.5%, Buan2 and Donglim3, 98.1%). For Gochang1 virus, polymerase basic protein 2 (PB2) and nonstructural (NS) protein had the highest identities with A/environment/Jiangxi/28/2009 (H11N9) (PB2 98.6%, NS 97.7%). The other segments showed high genetic identities with A/duck/Jiangsu/k1203/2010 (H5N8) (>98.7%), which suggested that Gochang1 virus was generated by reassortment in which the PB2 and NS genes of A/duck/Jiangsu/k1203/2010 (H5N8) were replaced by those of influenza A(H11N9) viruses. For Buan2 and Donglim3 viruses, the PB2, HA, nucleoprotein, and NA genes were highly similar to those of A/duck/Jiangsu/k1203/2010 (H5N8) (>97.2%). However, the PB1, polymerase acidic protein, matrix protein, and NS genes of this virus had the highest genetic identities with A/duck/Eastern China/1111/2011 (H5N2) (>98.2%). Therefore, Buan2 and Donglim3 viruses might be reassortants that contain PB2, HA, nucleoprotein, and NA genes from A/duck/Jiangsu/k1203/2010 (H5N8) and PB1, polymerase acidic protein, NS, and matrix genes from A/duck/Eastern China/1111/2011 (H5N2) co-circulating in the same region of China ( 2 , 10 ). We characterized 3 distinct novel reassortant influenza A(H5N8) HPAI viruses during an influenza outbreak in South Korea. Buan2 and Donglim3 viruses showed high nucleotide identities, which suggested that the outbreak viruses in domestic ducks and Baikal teals might have an identical origin. Although research on the epidemiologic features of this outbreak is currently underway, it seems likely that on the basis of reassortant sequence features of the 8 genome segments, the 3 distinct viruses originated in eastern China. These influenza viruses are a potential threat to the poultry population in South Korea, including gallinaceous birds, during movement of domestic ducks through the distribution network of live bird markets.
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            Highly pathogenic avian influenza virus (H5N8) in domestic poultry and its relationship with migratory birds in South Korea during 2014.

            Highly pathogenic H5N8 avian influenza viruses (HPAIVs) were introduced into South Korea during 2014, thereby caused outbreaks in wild birds and poultry farms. During the 2014 outbreak, H5N8 HPAIVs were isolated from 38 wild birds and 200 poultry farms (up to May 8, 2014). To better understand the introduction of these viruses and their relationships with wild birds and poultry farm, we analyzed the genetic sequences and available epidemiological data related to the viruses. Genetic analysis of 37 viruses isolated from wild birds and poultry farms showed that all of the isolates belonged to clade 2.3.4.6 of the hemagglutinin (HA) gene, but comprised two distinct groups. During the initial stage of the outbreak, identical isolates from each group were found in wild birds and poultry farms near Donglim Reservoir, which is a resting site for migratory birds, thereby indicating that two types of H5N8 HPAIVs were introduced into the lake at the same time. Interestingly, the one group of H5N8 HPAIV predominated around Donglim Reservoir, and the predominant virus was dispersed by wild birds among the migratory bird habitats in the western region of South Korea as time passed, and it was also detected in nearby poultry farms. Furthermore, compared with the results of the annual AIV surveillance of captured wild birds, which has been performed since 2008, more HPAIVs were isolated and H5 sero-prevalence was also detected during the 2014 outbreak. Overall, our results strongly suggest that migratory birds played a key role in the introduction and spread of viruses during the initial stage of the 2014 outbreak.
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              Characterization of three H5N5 and one H5N8 highly pathogenic avian influenza viruses in China.

              One H5N8 and three H5N5 highly pathogenic avian influenza (HPAI) viruses which derived their HA genes from the Asian H5N1 lineage were isolated from poultry during 2009-2010 in mainland China. Pathogenicity studies showed that these viruses were all highly virulent to chickens, while they varied from moderate to high virulence in mice and from mild to intermediate virulence in mallards. Phylogenetic analyses showed that these viruses were reassortants bearing the H5N1 backbone while acquiring PB1, NP and NA genes from unidentified non-H5N1 viruses, and had developed into three distinct genotypes (B-D). Molecular characterization indicated that all these viruses might resist to antiviral agents. Our findings highlight the emergence and development of HPAI H5 viruses of other NA subtypes in H5N1 endemic areas and their potential threat to poultry industry and public health. Copyright © 2013 Elsevier B.V. All rights reserved.
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                Author and article information

                Journal
                Influenza Other Respir Viruses
                Influenza Other Respir Viruses
                irv
                Influenza and Other Respiratory Viruses
                John Wiley & Sons, Ltd (Chichester, UK )
                1750-2640
                1750-2659
                September 2015
                04 August 2015
                : 9
                : 5
                : 271-276
                Affiliations
                [a ]Program of Emerging Infectious Diseases, Duke-NUS Graduate Medical School Singapore city, Singapore
                [b ]Influenza Division, Centers for Disease Control and Prevention Atlanta, GA, USA
                Author notes
                Correspondence: Gavin J.D. Smith, Program of Emerging Infectious Diseases, Duke-NUS Graduate Medical School, 169857, Singapore. E-mail: gavin.smith@ 123456duke-nus.edu.sg , Ruben O. Donis, Influenza Division, Centers for Disease Control and Prevention, MS G16, Atlanta, GA 30333, USA. E-mail: rvd6@ 123456cdc.gov
                [*]

                Group members and collaborators are provided in the Supporting Information ( Data S1).

                Article
                10.1111/irv.12324
                4548997
                25966311
                f2c1a92e-c37c-4b3d-ac49-d84c02e3f35a
                © 2015 The Authors. Influenza and Other Respiratory Viruses Published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 22 April 2015
                Categories
                Short Article

                Infectious disease & Microbiology
                clade nomenclature,h5 subtype,hemagglutinin,highly pathogenic avian influenza,molecular epidemiology,phylogenetics,viral evolution

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