Genesis, Evolution and Prevalence of H5N6 Avian Influenza Viruses in China

Yuhai Bi¹, Quanjiao Chen², Qianli Wang³, Jianjun Chen², Tao Jin⁴, Gary Wong⁵, Chuansong Quan⁶, Jun Liu⁶, Jun Wu³, Renfu Yin⁷, Lihua Zhao², Mingxin Li², Zhuang Ding⁷, Rongrong Zou⁸, Wen Xu⁹, Hong Li⁹, Huijun Wang¹⁰, Kegong Tian¹¹, Guanghua Fu¹², Yu Huang¹², Alexander Shestopalov¹³, Shoujun Li¹⁴, Bing Xu¹⁵, Hongjie Yu¹⁶, Tingrong Luo¹⁷, Lin Lu⁹, Xun Xu⁴, Yang Luo¹⁸, Yingxia Liu¹⁹, Weifeng Shi²⁰, Di Liu²¹, George Fu Gao²²

Affiliations

¹ Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Disease, Shenzhen Third People's Hospital, Shenzhen 518112, China; Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
² Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Hubei 430071, China.
³ Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
⁴ China National Genebank-Shenzhen, BGI-Shenzhen, Shenzhen 518083, China.
⁵ CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
⁶ National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention (China CDC), Beijing 102206, China.
⁷ Department of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Jilin 130062, China.
⁸ Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Disease, Shenzhen Third People's Hospital, Shenzhen 518112, China.
⁹ Yunnan Center for Disease Control and Prevention, Kunming 650022, China.
¹⁰ Diqing Tibetan Autonomous Prefecture Centers for Disease Control and Prevention, Shangri-la 674400, China.
¹¹ National Research Center for Veterinary Medicine, Luoyang 471003, China.
¹² Institute of Animal Husbandry and Veterinary Medicine, Fujian Academy of Agricultural Sciences, Fuzhou 350003, China.
¹³ Research Institute of Experimental and Clinical Medicine, Novosibirsk State University, Novosibirsk 630090, Russia.
¹⁴ College of Veterinary Medicine, South China Agricultural University, Guangzhou 510642, China.
¹⁵ Ministry of Education Key Laboratory for Earth System Modelling, Center for Earth System Science, Tsinghua University, Beijing 100084, China.
¹⁶ Division of Infectious Disease, Key Laboratory of Surveillance and Early-Warning on Infectious Disease, Chinese Center for Disease Control and Prevention, Beijing 102206, China.
¹⁷ Laboratory of Animal Infectious Diseases, College of Animal Sciences and Veterinary Medicine, Guangxi University, Nanning 530004, China.
¹⁸ Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA.
¹⁹ Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Disease, Shenzhen Third People's Hospital, Shenzhen 518112, China. Electronic address: yingxialiu@hotmail.com.
²⁰ Institute of Pathogen Biology, Taishan Medical College, Taian 271016, China. Electronic address: shiwf@ioz.ac.cn.
²¹ Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; Network Information Center, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China. Electronic address: liud@im.ac.cn.
²² Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Disease, Shenzhen Third People's Hospital, Shenzhen 518112, China; Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention (China CDC), Beijing 102206, China; Savaid Medical School, University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: gaof@im.ac.cn.

PMID: 27916476
DOI: 10.1016/j.chom.2016.10.022

Free article

Genesis, Evolution and Prevalence of H5N6 Avian Influenza Viruses in China

Yuhai Bi et al. Cell Host Microbe. 2016.

Free article

. 2016 Dec 14;20(6):810-821.

doi: 10.1016/j.chom.2016.10.022. Epub 2016 Dec 1.

Authors

Affiliations

¹ Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Disease, Shenzhen Third People's Hospital, Shenzhen 518112, China; Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
² Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Hubei 430071, China.
³ Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
⁴ China National Genebank-Shenzhen, BGI-Shenzhen, Shenzhen 518083, China.
⁵ CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
⁶ National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention (China CDC), Beijing 102206, China.
⁷ Department of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Jilin 130062, China.
⁸ Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Disease, Shenzhen Third People's Hospital, Shenzhen 518112, China.
⁹ Yunnan Center for Disease Control and Prevention, Kunming 650022, China.
¹⁰ Diqing Tibetan Autonomous Prefecture Centers for Disease Control and Prevention, Shangri-la 674400, China.
¹¹ National Research Center for Veterinary Medicine, Luoyang 471003, China.
¹² Institute of Animal Husbandry and Veterinary Medicine, Fujian Academy of Agricultural Sciences, Fuzhou 350003, China.
¹³ Research Institute of Experimental and Clinical Medicine, Novosibirsk State University, Novosibirsk 630090, Russia.
¹⁴ College of Veterinary Medicine, South China Agricultural University, Guangzhou 510642, China.
¹⁵ Ministry of Education Key Laboratory for Earth System Modelling, Center for Earth System Science, Tsinghua University, Beijing 100084, China.
¹⁶ Division of Infectious Disease, Key Laboratory of Surveillance and Early-Warning on Infectious Disease, Chinese Center for Disease Control and Prevention, Beijing 102206, China.
¹⁷ Laboratory of Animal Infectious Diseases, College of Animal Sciences and Veterinary Medicine, Guangxi University, Nanning 530004, China.
¹⁸ Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA.
¹⁹ Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Disease, Shenzhen Third People's Hospital, Shenzhen 518112, China. Electronic address: yingxialiu@hotmail.com.
²⁰ Institute of Pathogen Biology, Taishan Medical College, Taian 271016, China. Electronic address: shiwf@ioz.ac.cn.
²¹ Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; Network Information Center, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China. Electronic address: liud@im.ac.cn.
²² Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Disease, Shenzhen Third People's Hospital, Shenzhen 518112, China; Center for Influenza Research and Early-Warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention (China CDC), Beijing 102206, China; Savaid Medical School, University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: gaof@im.ac.cn.

PMID: 27916476
DOI: 10.1016/j.chom.2016.10.022

Abstract

Constant surveillance of live poultry markets (LPMs) is currently the best way to predict and identify emerging avian influenza viruses (AIVs) that pose a potential threat to public health. Through surveillance of LPMs from 16 provinces and municipalities in China during 2014-2016, we identified 3,174 AIV-positive samples and isolated and sequenced 1,135 AIVs covering 31 subtypes. Our analysis shows that H5N6 has replaced H5N1 as one of the dominant AIV subtypes in southern China, especially in ducks. Phylogenetic analysis reveals that H5N6 arose from reassortments of H5 and H6N6 viruses, with the hemagglutinin and neuraminidase combinations being strongly lineage specific. H5N6 viruses constitute at least 34 distinct genotypes derived from various evolutionary pathways. Notably, genotype G1.2 virus, with internal genes from the chicken H9N2/H7N9 gene pool, was responsible for at least five human H5N6 infections. Our findings highlight H5N6 AIVs as potential threats to public health and agriculture.

Keywords: H5N6 avian influenza; birds; evolution; genesis; human infection; live poultry markets; prevalence; resassortment.

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Genesis, Evolution and Prevalence of H5N6 Avian Influenza Viruses in China

Affiliations

Genesis, Evolution and Prevalence of H5N6 Avian Influenza Viruses in China

Authors

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Abstract

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Medical