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Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014.

Abstract

Four World Health Organization (WHO) Collaborating Centres for Reference and Research on Influenza and one WHO Collaborating Centre for the Surveillance, Epidemiology and Control of Influenza (WHO CCs) tested 10,641 viruses collected by WHO-recognized National Influenza Centres between May 2013 and May 2014 to determine 50% inhibitory concentration (IC50) data for neuraminidase inhibitors (NAIs) oseltamivir, zanamivir, peramivir and laninamivir. In addition, neuraminidase (NA) sequence data, available from the WHO CCs and from sequence databases (n=3206), were screened for amino acid substitutions associated with reduced NAI susceptibility. Ninety-five per cent of the viruses tested by the WHO CCs were from three WHO regions: Western Pacific, the Americas and Europe. Approximately 2% (n=172) showed highly reduced inhibition (HRI) against at least one of the four NAIs, commonly oseltamivir, while 0.3% (n=32) showed reduced inhibition (RI). Those showing HRI were A(H1N1)pdm09 with NA H275Y (n=169), A(H3N2) with NA E119V (n=1), B/Victoria-lineage with NA E117G (n=1) and B/Yamagata-lineage with NA H273Y (n=1); amino acid position numbering is A subtype and B type specific. Although approximately 98% of circulating viruses tested during the 2013-2014 period were sensitive to all four NAIs, a large community cluster of A(H1N1)pdm09 viruses with the NA H275Y substitution from patients with no previous exposure to antivirals was detected in Hokkaido, Japan. Significant numbers of A(H1N1)pdm09 NA H275Y viruses were also detected in China and the United States: phylogenetic analyses showed that the Chinese viruses were similar to those from Japan, while the United States viruses clustered separately from those of the Hokkaido outbreak, indicative of multiple resistance-emergence events. Consequently, global surveillance of influenza antiviral susceptibility should be continued from a public health perspective.

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  • Authors+Show Affiliations

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    World Health Organization Collaborating Centre for Reference and Research on Influenza, National Institute of Infectious Diseases, Gakuen 4-7-1, Musashimurayama, Tokyo 208-0011, Japan. Electronic address: emitaka@nih.go.jp.

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    National Institute for Public Health and the Environment, PO Box 1, 3720 BA Bilthoven, The Netherlands. Electronic address: adam.meijer@rivm.nl.

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    Public Health England Colindale, 61 Colindale Avenue, London NW9 5EQ, United Kingdom. Electronic address: Angie.Lackenby@phe.gov.uk.

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    World Health Organization Collaborating Centre for the Surveillance, Epidemiology and Control of Influenza, Centers for Disease Control and Prevention, 1600 Clifton RD NE, MS-G16 Atlanta, GA, United States. Electronic address: LGubareva@CDC.gov.

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    Instituto Nacional de Saúde, Av. Padre Cruz, 1649-016 Lisboa, Portugal; Faculdade de Farmácia, Universidade de Lisboa, Av. Prof. Gama Pinto, 1649-003 Lisboa, Portugal. Electronic address: h.rebelo.andrade@insa.min-saude.pt.

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    Global Influenza Programme, World Health Organization, Avenue Appia 20, 1211 Geneva 27, Switzerland. Electronic address: besselaart@who.int.

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    World Health Organization Collaborating Centre for the Surveillance, Epidemiology and Control of Influenza, Centers for Disease Control and Prevention, 1600 Clifton RD NE, MS-G16 Atlanta, GA, United States. Electronic address: agf1@cdc.gov.

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    World Health Organization Collaborating Centre for Reference and Research on Influenza, MRC-National Institute for Medical Research, The Ridgeway, Mill Hill, London NW7 1AA, United Kingdom. Electronic address: vgregor@nimr.mrc.ac.uk.

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    World Health Organization Collaborating Centre for Reference and Research on Influenza, VIDRL, At the Peter Doherty Institute for Infection and Immunity, Melbourne, VIC 3000, Australia. Electronic address: leah.leang@influenzacentre.org.

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    World Health Organization Collaborating Centre for Reference and Research on Influenza, Chinese National Influenza Center, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, 155 Changbai Road, Changping District, Beijing 102206, China. Electronic address: huangweijuan@cnic.org.cn.

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    Public Health Laboratory Centre, 382 Nam Cheong Street, Shek Kip Mei, Kowloon, Hong Kong, China. Electronic address: janicelo@dh.gov.hk.

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    Division of Communicable Diseases, Health Security, & Environment, World Health Organization Regional Office for Europe, UN City, Marmorvej 51, DK-2100 Copenhagen Ø, Denmark. Electronic address: PDM@euro.who.int.

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    Respiratory Viruses Laboratory/IOC, FIOCRUZ, Av Brasil, 4365 Rio de Janeiro, Brazil. Electronic address: mmsiq@ioc.fiocruz.br.

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    World Health Organization Collaborating Centre for Reference and Research on Influenza, Chinese National Influenza Center, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, 155 Changbai Road, Changping District, Beijing 102206, China. Electronic address: dayanwang@cnic.org.cn.

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    Public Health Laboratory Centre, 382 Nam Cheong Street, Shek Kip Mei, Kowloon, Hong Kong, China. Electronic address: so_phls10@dh.gov.hk.

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    Global Influenza Programme, World Health Organization, Avenue Appia 20, 1211 Geneva 27, Switzerland. Electronic address: zhangw@who.int.

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    World Health Organization Collaborating Centre for Reference and Research on Influenza, MRC-National Institute for Medical Research, The Ridgeway, Mill Hill, London NW7 1AA, United Kingdom. Electronic address: rdaniel@nimr.mrc.ac.uk.

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    World Health Organization Collaborating Centre for Reference and Research on Influenza, VIDRL, At the Peter Doherty Institute for Infection and Immunity, Melbourne, VIC 3000, Australia; University of Melbourne, Melbourne School of Population and Global Health, Melbourne, VIC 3010, Australia. Electronic address: Aeron.Hurt@influenzacentre.org.

    World Health Organization Collaborating Centre for Reference and Research on Influenza, National Institute of Infectious Diseases, Gakuen 4-7-1, Musashimurayama, Tokyo 208-0011, Japan. Electronic address: mtashiro2@gmail.com.

    Source

    Antiviral research 117: 2015 May pg 27-38

    MeSH

    Amino Acid Substitution
    Antiviral Agents
    China
    Cyclopentanes
    Disease Outbreaks
    Drug Resistance, Viral
    Enzyme Inhibitors
    Europe
    Guanidines
    Humans
    Influenza A Virus, H1N1 Subtype
    Influenza A Virus, H3N2 Subtype
    Influenza B virus
    Inhibitory Concentration 50
    Japan
    Microbial Sensitivity Tests
    Neuraminidase
    Oseltamivir
    Phylogeny
    Time Factors
    United States
    World Health Organization
    Zanamivir

    Pub Type(s)

    Journal Article
    Research Support, Non-U.S. Gov't

    Language

    eng

    PubMed ID

    25721488

    Citation

    Takashita, Emi, et al. "Global Update On the Susceptibility of Human Influenza Viruses to Neuraminidase Inhibitors, 2013-2014." Antiviral Research, vol. 117, 2015, pp. 27-38.
    Takashita E, Meijer A, Lackenby A, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014. Antiviral Res. 2015;117:27-38.
    Takashita, E., Meijer, A., Lackenby, A., Gubareva, L., Rebelo-de-Andrade, H., Besselaar, T., ... Tashiro, M. (2015). Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014. Antiviral Research, 117, pp. 27-38. doi:10.1016/j.antiviral.2015.02.003.
    Takashita E, et al. Global Update On the Susceptibility of Human Influenza Viruses to Neuraminidase Inhibitors, 2013-2014. Antiviral Res. 2015;117:27-38. PubMed PMID: 25721488.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014. AU - Takashita,Emi, AU - Meijer,Adam, AU - Lackenby,Angie, AU - Gubareva,Larisa, AU - Rebelo-de-Andrade,Helena, AU - Besselaar,Terry, AU - Fry,Alicia, AU - Gregory,Vicky, AU - Leang,Sook-Kwan, AU - Huang,Weijuan, AU - Lo,Janice, AU - Pereyaslov,Dmitriy, AU - Siqueira,Marilda M, AU - Wang,Dayan, AU - Mak,Gannon C, AU - Zhang,Wenqing, AU - Daniels,Rod S, AU - Hurt,Aeron C, AU - Tashiro,Masato, Y1 - 2015/02/23/ PY - 2014/11/24/received PY - 2015/01/28/revised PY - 2015/02/06/accepted PY - 2015/2/28/entrez PY - 2015/2/28/pubmed PY - 2016/1/21/medline KW - Antiviral resistance KW - Global analysis KW - Influenza virus KW - Neuraminidase inhibitors KW - Oseltamivir KW - Reduced susceptibility SP - 27 EP - 38 JF - Antiviral research JO - Antiviral Res. VL - 117 N2 - Four World Health Organization (WHO) Collaborating Centres for Reference and Research on Influenza and one WHO Collaborating Centre for the Surveillance, Epidemiology and Control of Influenza (WHO CCs) tested 10,641 viruses collected by WHO-recognized National Influenza Centres between May 2013 and May 2014 to determine 50% inhibitory concentration (IC50) data for neuraminidase inhibitors (NAIs) oseltamivir, zanamivir, peramivir and laninamivir. In addition, neuraminidase (NA) sequence data, available from the WHO CCs and from sequence databases (n=3206), were screened for amino acid substitutions associated with reduced NAI susceptibility. Ninety-five per cent of the viruses tested by the WHO CCs were from three WHO regions: Western Pacific, the Americas and Europe. Approximately 2% (n=172) showed highly reduced inhibition (HRI) against at least one of the four NAIs, commonly oseltamivir, while 0.3% (n=32) showed reduced inhibition (RI). Those showing HRI were A(H1N1)pdm09 with NA H275Y (n=169), A(H3N2) with NA E119V (n=1), B/Victoria-lineage with NA E117G (n=1) and B/Yamagata-lineage with NA H273Y (n=1); amino acid position numbering is A subtype and B type specific. Although approximately 98% of circulating viruses tested during the 2013-2014 period were sensitive to all four NAIs, a large community cluster of A(H1N1)pdm09 viruses with the NA H275Y substitution from patients with no previous exposure to antivirals was detected in Hokkaido, Japan. Significant numbers of A(H1N1)pdm09 NA H275Y viruses were also detected in China and the United States: phylogenetic analyses showed that the Chinese viruses were similar to those from Japan, while the United States viruses clustered separately from those of the Hokkaido outbreak, indicative of multiple resistance-emergence events. Consequently, global surveillance of influenza antiviral susceptibility should be continued from a public health perspective. SN - 1872-9096 UR - https://www.unboundmedicine.com/medline/citation/25721488/Global_update_on_the_susceptibility_of_human_influenza_viruses_to_neuraminidase_inhibitors_2013_2014_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0166-3542(15)00031-5 DB - PRIME DP - Unbound Medicine ER -