Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (20): 4075-4090.doi: 10.3864/j.issn.0578-1752.2022.20.017

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles    

Evolution of Human H9N2 Avian Influenza Virus in China from 1998 to 2021

WANG YanWen(),WANG MengJing,ZHANG Hong,GAO XinXin,GUO Jing(),LI XuYong()   

  1. College of Agronomy, Liaocheng University, Liaocheng 252000, Shandong
  • Received:2021-08-06 Accepted:2022-04-07 Online:2022-10-16 Published:2022-10-24
  • Contact: Jing GUO,XuYong LI E-mail:15290068938@163.com;guojing2360846@163.com;xylicaas@163.com

Abstract:

【Objective】 The epidemiological characteristics of H9N2 avian influenza virus were clarified by analyzing the onset time, province, age, gender and other information of human cases infected with H9N2 avian influenza from 1998 to 2021 in China. By analyzing the genetic characteristics of human H9N2 subtype avian influenza virus, the genetic evolution law of human H9N2 subtype avian influenza virus was elucidated. This study could provide data support for the early warning and control of H9N2 subtype avian influenza virus cross-species transmission. 【Method】 According to the case report, literature data and gene bank, the case information and strain sequence data of human infection with H9N2 subtype avian influenza virus in China from 1998 to 2021 were obtained. The infection cases were analyzed from the time distribution, space distribution, gender and age distribution, and the epidemiological characteristics of human-derived H9N2 subtype avian influenza virus infection were found. The MegAlign software in DNASTAR were used to analyze Nucleotide sequence of the homology of various gene fragments of human H9N2 isolates, a phylogenetic tree was constructed by MEGA7.0 software, and the key sites of viral proteins were analyzed. The genetic evolution trend of viral proteins and the variation of key amino acid sites were clarified. The 2019-2021 H9N2 subtype avian influenza virus nucleotide sequence in China was downloaded from the GISAID website. After mafft alignment, the key amino acid site mutation differences between human and avian H9N2 viruses were examined in MEGA7.0, the potential risks brought by current human and avian H9N2 viruses were revealed. 【Result】 From1998 to 2021, a total of 71 cases of human infection with the H9N2 subtype avian influenza virus occurred in China. From the spatial distribution analysis, the cases were distributed in 16 provinces and cities, of which 91.55% of the cases were from 12 provinces and cities in the south. In terms of time, the number of reported infections has been on the rise after 2013, and the cumulative number of infections from 2013 to 2021 accounted for 61.97% of the total number of infections. From the analysis of gender and age distribution, the ratio of male to female was 1:1.68. Human infection with H9N2 virus was mainly seen in infants and young children, accounting for 74.14% of the total number of cases. Genome comparison analysis of human H9N2 viruses found that these viruses belonged to the Eurasian branch, but the nucleotide sequence of homology of these viruses gene fragments was quite different. The nucleotide homology of HA, NA, PB2, PB1, PA, NP, M, and NS were 75.3%-100%, 80.1%-100%, 78.7%-100%, 82.5%-100%, 72.6%-100%, 74.1 -100%, 65.5%-100%, and 82.0%-100%, respectively. According to the genealogy of human isolates, 22 human isolates with complete gene fragments could be divided into 8 genotypes, genotypes in 2003, 2008, and 2013 were significantly different from genotypes in 1999. A total of 42 human H9N2 virus strains uploaded HA sequences from 1998 to 2021, and 38 of them had the mutation of Q226L in the HA protein; a total of 30 human virus strains uploaded PB2 sequence from 1998 to 2021, and 9 strains of which had the mutation of E627V in the PB2 protein, 1 of which had the mutation of E627K in the PB2 protein; the 701 site of the PB2 protein of one virus had the mutation of D701N, a total of 31 virus strains uploaded NS and M sequence from 1998 to 2021, the 42nd positions of the NS1 protein were all S, and the amino acids at positions 30th and 215th of the M1 protein were D and A, respectively. 【Conclusion】 Since 2013, the number of human infections with H9N2 subtype avian influenza reported in China has been on the rise, with significant differences in geographic, age and gender distribution. Since 1998, the genetic homology between human H9N2 isolates was quite different, and the viral gene rearrangement between different branches was frequent, forming a complex genotype. It was suggested that the H9N2 subtype avian influenza virus was constantly evolving. Mutations in key amino acid sites of human H9N2 virus and mutation rate of human viruses was higher than avian H9N2 viruses from 2019 to 2021, suggesting that the potential of H9N2 subtype avian influenza virus to infect humans was gradually increasing. This result enriched the knowledge of human H9N2 virus and provided an important reference for the prevention and control of H9N2 subtype avian influenza virus.

Key words: avian influenza virus, H9N2 subtype, epidemiology, genetic evolution: cross-species transmission

Fig. 1

Human infection with H9N2 AIV in China, 1998-2021 A: The spatial distribution of H9N2 subtype AIV cases in China; B: distribution of H9N2 subtype AIV case in China; C: distribution by age and sex of H9N2 subtype AIV case in China"

Fig. 2

The phylogenetic trees of HA and NA A: HA phylogenetic trees; B: NA phylogenetic trees"

Fig. 3

The phylogenetic trees of internal genes A: PB2 phylogenetic tree; B: PB1 phylogenetic tree; C: PA phylogenetic tree; D: NP phylogenetic tree; E: M phylogenetic tree; F: NS phylogenetic tree"

Fig. 4

Evolution of the genotypes of human H9N2 AIV from 1998 to 2021"

Table 1

The key amino acids substitution of H9N2 AIV"

人源H9N2分离株
Human H9N2 virus
HA PB2 NS1 M1
226 627 701 42 30 215
A/Shantou/239/1998(H9N2) Q - - - - -
A/Shaoguan/408/1998(H9N2) L - - - - -
A/Shaoguan/447/1998(H9N2) L - - - - -
A/Guangzhou/333/1999(H9N2) M E D S D A
A/Hongkong/1073/1999(H9N2) L E D S D A
A/Hongkong/1074/1999(H9N2) L E D S D A
A/Nanchang/CH2/2000(H9N2) L - - - - -
A/Nanchang/CH3/2000(H9N2) L - - - - -
A/Nanchang/D1/2000(H9N2) L - - - - -
A/Nanchang/D2/2000(H9N2) L - - - - -
A/Hongkong/2108/2003(H9N2) L E D S D A
A/Guangdong/W1/2004(H9N2) L E D S D A
A/Hongkong/3239/2008(H9N2) L E D S D A
A/Hongkong/69955/2008(H9N2) L - - - - -
A/Hongkong/33982/2009(H9N2) Q E N S D A
A/Hongkong/35820/2009(H9N2) Q - - S D A
A/Lengshuitan/11197/2013(H9N2) L E D S D A
A/Guangdong/167/2014(H9N2) - E D S D A
A/Guangdong/79/2015(H9N2) - E D S D A
A/Hunan/44557/2015(H9N2) L E D S D A
A/Hunan/44558/2015(H9N2) L E D S D A
A/Zhongshan/201501/2015(H9N2) L E D S D A
A/Beijing/1/2016(H9N2) L V D S D A
A/Guangdong/MZ058/2016(H9N2) L K D S D A
A/Beijing/1/2017(H9N2) L V D S D A
A/Hunan/37286/2017(H9N2) L V D S D A
A/Hunan/42088/2017(H9N2) L V D S D A
A/Hunan/34179/2018(H9N2) L V D S D A
A/Guangxi/11522/2018(H9N2) L E D S D A
A/Anhui/39/2018(H9N2) L V D S D A
A/Guangdong/18SF003/2018(H9N2) L E D S D A
A/Guangdong/18SF064/2018(H9N2) L E D S D A
A/Fujian/2881/2019(H9N2) L V D S D A
A/Hubei/1187/2019(H9N2) L V D S D A
A/Hubei/1317/2019(H9N2) L V D S D A
A/Hubei/1423/2019(H9N2) L E D S D A
A/Hubei/1534/2019(H9N2) L V D S D A
A/Hubei/1565/2019(H9N2) L V D S D A
A/Hubei/1631/2019(H9N2) L - - - - -
A/Hubei/1693/2019(H9N2) L V D S D A
A/Hubei/1803/2019(H9N2) L V D S D A
A/Hubei/2081/2019(H9N2) L V D S D A
A/Hubei/2280/2019(H9N2) L E D S D A
A/Hubei/2299/2019(H9N2) L V D S D A
A/Hubei/2370/2019(H9N2) L V D S D A
A/Hubei/239/2019(H9N2) L E D S D A
A/Hubei/2462/2019(H9N2) L E D S D A
A/Hubei/2542/2019(H9N2) L E D S D A
A/Hubei/295/2019(H9N2) L V D S D A
A/Hubei/362/2019(H9N2) L E D S D A
A/Suzhou/GIRD01/2019(H9N2) L E D S D A
A/Fujian/1348/2020(H9N2) L E D S D A
A/Guangdong/20SF8034/2020(H9N2) L E D S - -
A/Guangdong/SF1634/2020(H9N2) L - - - - -
A/Guangdong/20SF15010/2020(H9N2) L - - - - -
A/Guangdong/11172/2020(H9N2) L E D S D A
A/Guizhou/13392/2020(H9N2) L - - - - -
A/Hunan/11173/2020(H9N2) L V D S D A
A/Shandong/01/2020(H9N2) L V D S D A
A/Sichuan/1619/2020(H9N2) L - - - - -

Fig. 5

Statistical analysis of the amino acids mutation of H9N2 AIV isolated from 2019 to 2021 A: Distribution of key amino acid sites of poultry H9N2 subtype AIV in China from 2019 to 2021; B: Distribution of key amino acid sites of human H9N2 subtype AIV in China from 2019 to 2021"

[1] HOMME P J, EASTERDAY B C. Avian influenza virus infections. I. Characteristics of influenza A-Turkey-Wisconsin-1966 virus. Avian Diseases, 1970, 14(1): 66-74.
pmid: 4314007
[2] ZHONG L, WANG X Q, LI Q H, LIU D, CHEN H Z, ZHAO M J, GU X B, HE L, LIU X W, GU M, PENG D X, LIU X F. Molecular mechanism of the airborne transmissibility of H9N2 avian influenza A viruses in chickens. Journal of Virology, 2014, 88(17): 9568-9578. doi: 10.1128/JVI.00943-14.
doi: 10.1128/JVI.00943-14 pmid: 24920791
[3] ZHANG P H, TANG Y H, LIU X W, PENG D X, LIU W B, LIU H Q, LU S, LIU X F. Characterization of H9N2 influenza viruses isolated from vaccinated flocks in an integrated broiler chicken operation in Eastern China during a 5 year period (1998-2002). The Journal of General Virology, 2008, 89(Pt12): 3102-3112. doi: 10.1099/vir.0.2008/005652-0.
doi: 10.1099/vir.0. 2008/005652-0
[4] SUN Y P, LIU J H. H9N2 influenza virus in China: a cause of concern. Protein & Cell, 2015, 6(1): 18-25. doi: 10.1007/s13238-014-0111-7.
doi: 10.1007/s13238-014-0111-7
[5] PEACOCK T H P, JAMES J, SEALY J E, IQBAL M. A global perspective on H9N2 avian influenza virus. Viruses, 2019, 11(7): 620. doi: 10.3390/v11070620.
doi: 10.3390/v11070620
[6] HE J, LIU B Y, GONG L, CHEN Z, CHEN X L, HOU S, YU J L, WU J B, XIA Z C, LATIF A, GAO R, SU B, LIU Y. Genetic characterization of the first detected human case of avian influenza A (H5N6) in Anhui Province, East China. Scientific Reports, 2018, 8: 15282. doi: 10.1038/s41598-018-33356-4.
doi: 10.1038/s41598-018-33356-4 pmid: 30327485
[7] ZHANG Q Y, SHI J Z, DENG G H, GUO J, ZENG X Y, HE X J, KONG H H, GU C Y, LI X Y, LIU J X, WANG G J, CHEN Y, LIU L L, LIANG L B, LI Y Y, FAN J, WANG J L, LI W H, GUAN L Z, LI Q M, YANG H L, CHEN P C, JIANG L, GUAN Y T, XIN X G, JIANG Y P, TIAN G B, WANG X R, QIAO C L, LI C J, BU Z G, CHEN H L. H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science, 2013, 341(6144): 410-414. doi: 10.1126/science.1240532.
doi: 10.1126/science.1240532 pmid: 23868922
[8] LI X Y, CUI P F, ZENG X Y, JIANG Y P, LI Y B, YANG J X, PAN Y D, GAO X X, ZHAO C H, WANG J H, WANG K, DENG G H, GUO J. Characterization of avian influenza H5N3 reassortants isolated from migratory waterfowl and domestic ducks in China from 2015 to 2018. Transboundary and Emerging Diseases, 2019, 66(6): 2605-2610. doi: 10.1111/tbed.13324.
doi: 10.1111/tbed.13324 pmid: 31402584
[9] CHEN H Y, YUAN H, GAO R B, ZHANG J X, WANG D Y, XIONG Y, FAN G Y, YANG F, LI X D, ZHOU J F, ZOU S M, YANG L, CHEN T, DONG L B, BO H, ZHAO X, ZHANG Y, LAN Y, SHU Y L. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. The Lancet, 2014, 383(9918):714-721. doi:10.1016/S0140-6736(14) 60111-2.
doi: 10.1016/S0140-6736(14)60111-2
[10] YU X F, JIN T, CUI Y J, PU X Y, LI J, XU J, LIU G, JIA H J, LIU D, SONG S L, YU Y, XIE L, HUANG R J, DING H, KOU Y, ZHOU Y Y, WANG Y Y, XU X, YIN Y, WANG J, GUO C Y, YANG X W, HU L P, WU X P, WANG H L, LIU J, ZHAO G Q, ZHOU J Y, PAN J C, GAO G F, YANG R F, WANG J. Influenza H7N9 and H9N2 viruses: coexistence in poultry linked to human H7N9 infection and genome characteristics. Journal of Virology, 2014, 88(6): 3423-3431. doi: 10.1128/JVI.02059-13.
doi: 10.1128/JVI.02059-13 pmid: 24403589
[11] KANDEIL A, EL-SHESHENY R, MAATOUQ A M, MOATASIM Y, SHEHATA M M, BAGATO O, RUBRUM A, SHANMUGANATHAM K, WEBBY R J, ALI M A, KAYALI G. Genetic and antigenic evolution of H9N2 avian influenza viruses circulating in Egypt between 2011 and 2013. Archives of Virology, 2014, 159(11): 2861-2876. doi: 10.1007/s00705-014-2118-z.
doi: 10.1007/s00705-014-2118-z pmid: 24990416
[12] LIN Y P, SHAW M, GREGORY V, CAMERON K, LIM W, KLIMOV A, SUBBARAO K, GUAN Y, KRAUSS S, SHORTRIDGE K, WEBSTER R, COX N, HAY A. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97(17): 9654-9658. doi: 10.1073/pnas.160270697.
doi: 10.1073/pnas.160270697 pmid: 10920197
[13] LV J, WEI B Z, YANG Y, YAO M L, CAI Y M, GAO Y W, XIA X Z, ZHAO X N, LIU Z H, LI X X, WANG H, YANG H L, ROESLER U, MIAO Z M, CHAI T J. Experimental transmission in Guinea pigs of H9N2 avian influenza viruses from indoor air of chicken houses. Virus Research, 2012, 170(1/2): 102-108. doi: 10.1016/j.virusres.2012.09.003.
doi: 10.1016/j.virusres.2012. 09.003
[14] ZHANG K, ZHANG Z W, YU Z J, LI L, CHENG K H, WANG T C, HUANG G, YANG S T, ZHAO Y K, FENG N, FU J, QIN C, GAO Y W, XIA X Z. Domestic cats and dogs are susceptible to H9N2 avian influenza virus. Virus Research, 2013, 175(1): 52-57. doi: 10.1016/j.virusres.2013.04.004.
doi: 10.1016/j.virusres.2013.04.004 pmid: 23603563
[15] ZHU Y C, ZHANG B, SUN Z H, WANG X J, FAN X H, GAO L X, LIANG Y, CHEN X Y, ZHANG Z F. Replication and pathology of duck influenza virus subtype H9N2 in chukar. Biomedical and Environmental Sciences, 2018, 31(4): 306-310. doi: 10.3967/bes2018.039.
doi: 10.3967/bes2018.039 pmid: 29773094
[16] ALI M, YAQUB T, MUKHTAR N, IMRAN M, GHAFOOR A, SHAHID M F, NAEEM M, IQBAL M, SMITH G J D, SU Y C F. Avian influenza A(H9N2) virus in poultry worker, Pakistan, 2015. Emerging Infectious Diseases, 2019, 25(1): 136-139. doi: 10.3201/eid2501.180618.
doi: 10.3201/eid2501.180618 pmid: 30561309
[17] NAGY A, METTENLEITER T C, ABDELWHAB E M. A brief summary of the epidemiology and genetic relatedness of avian influenza H9N2 virus in birds and mammals in the Middle East and North Africa. Epidemiology and Infection, 2017, 145(16): 3320-3333. doi: 10.1017/S0950268817002576.
doi: 10.1017/S0950268817002576 pmid: 29168447
[18] 孙莹, 张兵, 李岭, 黄小洁, 侯力丹, 刘丹, 李启红, 李俊平, 王乐元, 李慧姣, 杨承槐. 表达H9亚型禽流感病毒HA基因重组鸭肠炎病毒的构建. 中国农业科学, 2019, 52(23): 4398-4405. doi: 10.3864/j.issn.0578-1752.2019.23.020.
doi: 10. 3864/j.issn.0578-1752.2019.23.020
SUN Y, ZHANG B, LI L, HUANG X J, HOU L D, LIU D, LI Q H, LI J P, WANG L Y, LI H J, YANG C H. Construction of a recombinant duck enteritis virus expressing hemagglutinin of H9N2 avian influenza virus. Scientia Agricultura Sinica, 2019, 52(23): 4398-4405. doi: 10.3864/j.issn.0578-1752.2019.23.020. (in Chinese)
doi: 10. 3864/j.issn.0578-1752.2019.23.020
[19] 丁洁, 高玉伟, 桑晓宇, 程凯慧, 于志君, 张坤, 柴洪亮, 王铁成, 夏咸柱, 华育平. H9N2亚型AIV鼠肺适应株的获得及其氨基酸变异分析. 中国农业科学, 2015, 48(15): 3056-3063.
DING J, GAO Y W, SANG X Y, CHENG K H, YU Z J, ZHANG K, CHAI H L, WANG T C, XIA X Z, HUA Y P. The adaptation of H9N2 subtype AIV in mouse and analysis of amino acid mutation. Scientia Agricultura Sinica, 2015, 48(15): 3056-3063. (in Chinese)
[20] LU J H, LIU X F, SHAO W X, LIU Y L, WEI D P, LIU H Q. Phylogenetic analysis of eight genes of H9N2 subtype influenza virus: a mainland China strain possessing early isolates' genes that have been circulating. Virus Genes, 2005, 31(2): 163-169. doi: 10.1007/s11262-005-1790-1.
doi: 10.1007/s11262- 005-1790-1
[21] FUSARO A, MONNE I, SALVIATO A, VALASTRO V, SCHIVO A, AMARIN N M, GONZALEZ C, ISMAIL M M, AL-ANKARI A R, AL-BLOWI M H, KHAN O A, MAKEN ALI A S, HEDAYATI A, GARCIA GARCIA J, ZIAY G M, SHOUSHTARI A, AL QAHTANI K N, CAPUA I, HOLMES E C, CATTOLI G. Phylogeography and evolutionary history of reassortant H9N2 viruses with potential human health implications. Journal of Virology, 2011, 85(16): 8413-8421. doi: 10.1128/JVI.00219-11.
doi: 10.1128/JVI.00219-11 pmid: 21680519
[22] XU K M, SMITH G J D, BAHL J, DUAN L, TAI H, VIJAYKRISHNA D, WANG J, ZHANG J X, LI K S, FAN X H, WEBSTER R G, CHEN H, PEIRIS J S M, GUAN Y. The genesis and evolution of H9N2 influenza viruses in poultry from Southern China, 2000 to 2005. Journal of Virology, 2007, 81(19): 10389-10401. doi: 10.1128/JVI.00979-07.
doi: 10.1128/JVI.00979-07 pmid: 17652402
[23] SUN X J, BELSER J A, MAINES T R. Adaptation of H9N2 influenza viruses to mammalian hosts: a review of molecular markers. Viruses, 2020, 12(5): 541. doi: 10.3390/v12050541.
doi: 10.3390/v12050541
[24] SORRELL E M, WAN H Q, ARAYA Y, SONG H C, PEREZ D R. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(18): 7565-7570. doi: 10.1073/pnas.0900877106.
doi: 10.1073/pnas.0900877106 pmid: 19380727
[25] WAN H Q, PEREZ D R. Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. Journal of Virology, 2007, 81(10): 5181-5191. doi: 10.1128/JVI.02827-06.
doi: 10.1128/JVI.02827-06 pmid: 17344280
[26] GABRIEL G, HERWIG A, KLENK H D. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathogens, 2008, 4(2): e11. doi: 10.1371/journal.ppat.0040011.
doi: 10. 1371/journal.ppat.0040011
[27] ZHANG H, LI X Y, GUO J, LI L, CHANG C, LI Y Y, BIAN C, XU K, CHEN H L, SUN B. The PB2 E627K mutation contributes to the high polymerase activity and enhanced replication of H7N9 influenza virus. The Journal of General Virology, 2014, 95(Pt 4): 779-786. doi: 10.1099/vir.0.061721-0.
doi: 10. 1099/vir.0.061721-0
[28] GU M, XU L J, WANG X Q, LIU X F. Current situation of H9N2 subtype avian influenza in China. Veterinary Research, 2017, 48(1): 49. doi: 10.1186/s13567-017-0453-2.
doi: 10.1186/s13567-017-0453-2 pmid: 28915920
[29] LI C, WANG S G, BING G X, CARTER R A, WANG Z J, WANG J L, WANG C X, WANG L, WU G, WEBSTER R G, WANG Y Q, SUN H L, SUN Y P, LIU J H, PU J. Genetic evolution of influenza H9N2 viruses isolated from various hosts in China from 1994 to 2013. Emerging Microbes & Infections, 2017, 6(1): 1-11. doi: 10.1038/emi.2017.94.
doi: 10.1038/emi. 2017.94
[30] LI X Y, LIU B T, MA S J, CUI P F, LIU W Q, LI Y B, GUO J, CHEN H L. High frequency of reassortment after co-infection of chickens with the H4N6 and H9N2 influenza A viruses and the biological characteristics of the reassortants. Veterinary Microbiology, 2018, 222: 11-17. doi: 10.1016/j.vetmic.2018.06.011.
doi: S0378-1135(17)31466-9 pmid: 30080665
[31] KIMBLE J B, SORRELL E, SHAO H X, MARTIN P L, PEREZ D R. Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(29): 12084-12088. doi: 10.1073/pnas.1108058108.
doi: 10.1073/pnas.1108058108 pmid: 21730147
[32] HU Z B, PENG F H, XIONG Z H, ZHANG W P, LI T T, SHI Y J, XIE J, JIN X, HUANG J J, XIAO H D, BI D R, SONG N H, LI Z L. Genetic and molecular characterization of H9N2 avian influenza viruses isolated from live poultry markets in Hubei Province, central China, 2013-2017. Virologica Sinica, 2021, 36(2): 291-299. doi: 10.1007/s12250-020-00260-z.
doi: 10. 1007/s12250-020-00260-z
[33] 庄丽, 王恒, 冯蓓, 蒋琳, 蒋维佳. 贵州省首次报道人感染H9N2禽流感病例的病原学诊断及意义. 贵州医药, 2019, 43(4): 617-618. doi: 10.3969/j.issn.1000-744X.2019.04.044.
doi: 10.3969/j.issn.1000-744X.2019.04.044
ZHUANG L, WANG H, FENG B, JIANG L, JIANG W J. The etiological diagnosis and significance of a human case of H9N2 avian influenza reported in Guizhou Province for the first time. Guizhou Medical Journal, 2019, 43(4): 617-618. doi: 10.3969/j.issn.1000-744X.2019.04.044. (in Chinese)
doi: 10.3969/j.issn.1000-744X.2019.04.044
[34] 朱汝南, 孙宇, 王芳, 赵林清, 邓洁, 田润, 钱渊. 北京儿童中发现人感染禽流感病毒H9N2病例一例. 中华儿科杂志, 2017, 55(1): 69. doi: 10.3760/cma.j.issn.0578-1310.2017.01.016.
doi: 10.3760/cma.j.issn.0578-1310.2017.01.016
ZHU R N, SUN Y, WANG F, ZHAO L Q, DENG J, TIAN R, QIAN Y. A case of human infection with avian influenza virus H9N2 was found in a Beijing child. Chinese Journal of Pediatrics, 2017, 55(1): 69. doi: 10.3760/cma.j.issn.0578-1310.2017.01.016. (in Chinese)
doi: 10.3760/cma.j.issn.0578-1310.2017.01.016
[35] 张斯钰, 黄一伟, 胡世雄, 张恒娇, 孙倩莱, 邓志红, 曾舸, 张红, 湛志飞, 高立冬. 湖南省2005—2017年人感染禽流感流行病学特征分析. 中华疾病控制杂志, 2018, 22(10): 1037-1040. doi: 10.16462/j.cnki.zhjbkz.2018.10.014.
doi: 10. 16462/j.cnki.zhjbkz.2018.10.014
ZHANG S Y, HUANG Y W, HU S X, ZHANG H J, SUN Q L, DENG Z H, ZENG G, ZHANG H, ZHAN Z F, GAO L D. Epidemiologic characteristics of human avian influenza in Hunan Province from 2005 to 2017. Chinese Journal of Disease Control & Prevention, 2018, 22(10): 1037-1040. doi: 10.16462/j.cnki.zhjbkz.2018.10.014. (in Chinese)
doi: 10. 16462/j.cnki.zhjbkz.2018.10.014
[36] 杨磊, 杜训波, 张晓春, 岳勇, 翁贵武, 昝宇, 韩德琳. 成都市首例人感染H9N2禽流感病例调查与分析. 中国人兽共患病学报, 2017, 33(3): 245-249. doi: 10.3969/j.issn.1002-2694.2017.03.010.
doi: 10.3969/j.issn.1002-2694.2017.03.010
YANG L, DU X B, ZHANG X C, YUE Y, WENG G W, ZAN Y, HAN D L. Investigation and analysis of the first cases of human infection with avian influenza A(H9N2) virus in Chengdu, China. Chinese Journal of Zoonoses, 2017, 33(3): 245-249. doi: 10.3969/j.issn.1002-2694.2017.03.010. (in Chinese)
doi: 10.3969/j.issn.1002-2694.2017.03.010
[37] 罗春蕊, 赵晓南, 宁德明, 李多, 徐闻. 云南省首例人感染H9N2禽流感病例发现与应对. 中国人兽共患病学报, 2017, 33(3): 241-244. doi: 10.3969/j.issn.1002-2694.2017.03.009.
doi: 10.3969/j.issn.1002-2694.2017.03.009
LUO C R, ZHAO X N, NING D M, LI D, XU W. Discovery and response of the first case of human infection with avian influenza A(H9N2) virus in Yunnan Province, China. Chinese Journal of Zoonoses, 2017, 33(3): 241-244. doi: 10.3969/j.issn.1002-2694.2017.03.009. (in Chinese)
doi: 10.3969/j.issn.1002-2694.2017.03.009
[38] 刘峰, 李刚, 刘凤仁, 俞国龙. 广东省深圳市首例孕妇感染H9N2禽流感病例流行病学调查. 疾病监测, 2019, 34(7): 621-625. doi: 10.3784/j.issn.1003-9961.2019.07.010.
doi: 10.3784/j.issn.1003-9961.2019.07.010
LIU F, LI G, LIU F R, YU G L. Epidemiological survey of the first case of pregnant women infection with avian influenza A (H9N2) virus in Shenzhen. Disease Surveillance, 2019, 34(7): 621-625. doi: 10.3784/j.issn.1003-9961.2019.07.010. (in Chinese)
doi: 10.3784/j.issn.1003-9961.2019.07.010
[39] 黄政, 欧新华, 袁洁, 刘晓蕾. 长沙市首例人感染H9N2禽流感病毒的HA基因序列特征分析. 中国人兽共患病学报, 2016, 32(11): 997-1000. doi: 10.3969/j.issn.1002-2694.2016.011.010.
doi: 10.3969/j.issn.1002-2694.2016.011.010
HUANG Z, OU X H, YUAN J, LIU X L. Isolation and characteristic analysis of an avian influenza virus (H9N2) from a patient in Changsha, China. Chinese Journal of Zoonoses, 2016, 32(11): 997-1000. doi: 10.3969/j.issn.1002-2694.2016.011.010. (in Chinese)
doi: 10.3969/j.issn.1002-2694.2016.011.010
[40] 何军, 刘丽萍, 侯赛, 龚磊, 吴家兵, 胡万富, 王建军. 安徽省2株人感染H9N2流感病毒基因特征. 中华流行病学杂志, 2016, 37(5): 708-713.
HE J, LIU L P, HOU S, GONG L, WU J B, HU W F, WANG J J. Genetic characteristics of two human H9N2 influenza virus strains in Anhui Province. Chinese Journal of Epidemiology, 2016, 37(5): 708-713. (in Chinese)
[41] 郭元吉, 李建国, 程小雯, 王敏, 邹毅, 李钏华, 蔡访潺, 廖华乐, 张烨, 郭俊峰, 黄瑞敏, 贝东. 禽H9N2亚型流感病毒能感染人的发现. 中华实验和临床病毒学杂志, 1999, 13(2): 105.
GUO Y J, LI J G, CHENG X W, WANG M, ZOU Y, LI C H, CAI F C, LIAO H L, ZHANG Y, GUO J F, HUANG R M, BEI D. Discovery of men infected by avian influenza A(H9N2) virus. Chinese Journal of Experimental and Clinical Virology, 1999, 13(2): 105. (in Chinese)
[42] BUTT K M, SMITH G J D, CHEN H L, ZHANG L J, LEUNG Y H C, XU K M, LIM W, WEBSTER R G, YUEN K Y, PEIRIS J S M, GUAN Y. Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. Journal of Clinical Microbiology, 2005, 43(11): 5760-5767. doi: 10.1128/JCM.43.11.5760-5767.2005.
doi: 10.1128/JCM.43.11.5760-5767.2005 pmid: 16272514
[43] SONG W J, QIN K. Human-infecting influenza A (H9N2) virus: a forgotten potential pandemic strain? Zoonoses and Public Health, 2020, 67(3): 203-212. doi: 10.1111/zph.12685.
doi: 10.1111/zph.12685 pmid: 31930694
[44] DONG X, XIONG J S, HUANG C L, XIANG J, WU W J, CHEN N S, WEN D N, TU C, QIAO X L, KANG L, YAO Z Z, ZHANG D Y, CHEN Q J. RETRACTED ARTICLE: human H9N2 avian influenza infection: epidemiological and clinical characterization of 16 cases in China. Virologica Sinica, 2021, 36(3): 564. doi: 10.1007/s12250-020-00248-9.
doi: 10.1007/s12250-020- 00248-9
[45] 尹馨, 马树杰, 李梅, 邓国华, 侯玉杰, 崔鹏飞, 施建忠, 陈化兰. PB2蛋白E627V突变可增强H7N9病毒对小鼠的致病力. 中国农业科学, 2018, 51(17): 3379-3388. doi: 10.3864/j.issn.0578-1752.2018.17.012.
doi: 10.3864/j.issn.0578-1752. 2018.17.012
YIN X, MA S J, LI M, DENG G H, HOU Y J, CUI P F, SHI J Z, CHEN H L. Amino acid substitutions of E627V in polymerase basic protein 2 gene increases the pathogenicity of the H7N9 influenza virus in mice. Scientia Agricultura Sinica, 2018, 51(17): 3379-3388. doi: 10.3864/j.issn.0578-1752.2018.17.012. (in Chinese)
doi: 10.3864/j.issn.0578-1752. 2018.17.012
[46] HUANG Y Y, HU B X, WEN X T, CAO S J, GAVRILOV B K, DU Q J, KHAN M I, ZHANG X M. Diversified reassortant H9N2 avian influenza viruses in chicken flocks in northern and Eastern China. Virus Research, 2010, 151(1): 26-32. doi: 10.1016/j.virusres.2010.03.010.
doi: 10.1016/j.virusres.2010.03.010 pmid: 20347894
[47] 乐高钟, 吴小秧, 易爱兰, 罗勤, 冯秀, 游胜. 江西省首例儿童禽流感H9N2亚型病例的调查分析. 现代预防医学, 2017, 44(5): 785-787, 792.
YUE G Z, WU X Y, YI A L, LUO Q, FENG X, YOU S. The first case of children & #39;s H9N2 subtype avian influenza in Jiangxi Province. Modern Preventive Medicine, 2017, 44(5): 785-787, 792. (in Chinese)
[48] PUSCH E A, SUAREZ D L. The multifaceted zoonotic risk of H9N2 avian influenza. Veterinary Sciences, 2018, 5(4): 82. doi: 10.3390/vetsci5040082.
doi: 10.3390/ vetsci5040082
[49] ZHANG P H, TANG Y H, LIU X W, LIU W B, ZHANG X R, LIU H Q, PENG D X, GAO S, WU Y T, ZHANG L Y, LU S, LIU X F. A novel genotype H9N2 influenza virus possessing human H5N1 internal genomes has been circulating in poultry in Eastern China since 1998. Journal of Virology, 2009, 83(17): 8428-8438. doi: 10.1128/JVI.00659-09.
doi: 10.1128/JVI.00659-09 pmid: 19553328
[50] LIU H Q, LIU X F, CHENG J, PENG D X, JIA L J, HUANG Y. Phylogenetic analysis of the hemagglutinin genes of twenty-six avian influenza viruses of subtype H9N2 isolated from chickens in China during 1996-2001. Avian Diseases, 2003, 47(1): 116-127. doi: 10.1637/0005-2086(2003)047[0116:PAOTHG]2.0.CO;2.
doi: 10. 1637/0005-2086(2003)047[0116: PAOTHG]2.0.CO pmid: 12713166
[51] ZHU R, XU D W, YANG X Q, ZHANG J J, WANG S F, SHI H Y, LIU X F. Genetic and biological characterization of H9N2 avian influenza viruses isolated in China from 2011 to 2014. PLoS ONE, 2018, 13(7): e0199260. doi: 10.1371/journal.pone.0199260.
doi: 10.1371/journal.pone.0199260
[52] LI X Y, SHI J Z, GUO J, DENG G H, ZHANG Q Y, WANG J L, HE X J, WANG K C, CHEN J M, LI Y Y, FAN J, KONG H, GU C Y, GUAN Y T, SUZUKI Y, KAWAOKA Y, LIU L L, JIANG Y P, TIAN G B, LI Y B, BU Z G, CHEN H L. Genetics, receptor binding property, and transmissibility in mammals of naturally isolated H9N2 Avian Influenza viruses. PLoS Pathogens, 2014, 10(11): e1004508. doi: 10.1371/journal.ppat.1004508.
doi: 10. 1371/journal.ppat.1004508
[53] LIU X K, YANG C, SUN X M, LIN X, ZHAO L Z, CHEN H C, JIN M L. Evidence for a novel mechanism of influenza A virus host adaptation modulated by PB2-627. The FEBS Journal, 2019, 286(17): 3389-3400. doi: 10.1111/febs.14867.
doi: 10.1111/febs.14867
[54] 张静, 陈立根, 张宇, 孙乾晋, 李如意, 白牧原, 蔺文成, 谢青梅. 1997—2015年我国不同地区H9N2亚型禽流感病毒流行情况研究. 中国家禽, 2016, 38(20): 20-27. doi: 10.16372/j.issn.1004-6364.2016.20.005.
doi: 10.16372/j.issn.1004-6364.2016. 20.005
ZHANG J, CHEN L G, ZHANG Y, SUN Q J, LI R Y, BAI M Y, LIN W C, XIE Q M. Prevalence of H9N2 subtype avian influenza virus in different regions of China during 1997 to 2015. China Poultry, 2016, 38(20): 20-27. doi: 10.16372/j.issn.1004-6364.2016.20.005. (in Chinese)
doi: 10.16372/j.issn.1004-6364.2016. 20.005
[55] JIAO P R, TIAN G B, LI Y B, DENG G H, JIANG Y P, LIU C, LIU W L, BU Z G, KAWAOKA Y, CHEN H L. A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. Journal of Virology, 2008, 82(3): 1146-1154. doi: 10.1128/jvi.01698-07.
doi: 10.1128/jvi.01698-07
[56] FAN S F, DENG G H, SONG J S, TIAN G B, SUO Y B, JIANG Y P, GUAN Y T, BU Z G, KAWAOKA Y, CHEN H L. Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. Virology, 2009, 384(1): 28-32. doi: 10.1016/j.virol.2008.11.044.
doi: 10.1016/j.virol.2008.11.044 pmid: 19117585
[57] 王云鹤, 包红梅, 孙佳善, 李雁冰, 徐晓龙, 王子龙, 施建忠, 曾显营, 王秀荣, 陈化兰. H7N9亚型禽流感病毒RT-PCR检测方法建立. 中国农业科学, 2015, 48(15): 3050-3055.
WANG Y H, BAO H M, SUN J S, LI Y B, XU X L, WANG Z L, SHI J Z, ZENG X Y, WANG X R, CHEN H L. Development of RT-PCR technique for detection of H7N9 subtype avian influenza virus. Scientia Agricultura Sinica, 2015, 48(15): 3050-3055. (in Chinese)
[58] 王萍萍, 郭晶, 李玉保, 刘成, 李旭勇. H7N9亚型禽流感病毒研究进展. 中国人兽共患病学报, 2021, 37(2): 159-164, 170. doi: 10.3969/j.issn.1002-2694.2021.00.010.
doi: 10. 3969/j.issn.1002-2694.2021.00.010
WANG P P, GUO J, LI Y B, LIU C, LI X Y. Research progress in H7N9 subtype avian influenza viruses. Chinese Journal of Zoonoses, 2021, 37(2): 159-164, 170. doi: 10.3969/j.issn.1002-2694.2021.00.010. (in Chinese)
doi: 10. 3969/j.issn.1002-2694.2021.00.010
[59] 辛丽, 白天, 周剑芳, 唐静, 陈永坤, 陈涛, 史景红, 李晓丹, 李燕. 中国职业暴露人群感染H9N2禽流感病毒血清学调查. 疾病监测, 2015, 30(5): 368-371. doi: 10.3784/j.issn.1003-9961.2015.05.007.
doi: 10.3784/j.issn.1003-9961.2015.05.007
XIN L, BAI T, ZHOU J F, TANG J, CHEN Y K, CHEN T, SHI J H, LI X D, LI Y. Serological study of human infection with avian influenza A (H9N2) virus in population with occupational exposure in China. Disease Surveillance, 2015, 30(5): 368-371. doi: 10.3784/j.issn.1003-9961.2015.05.007. (in Chinese)
doi: 10.3784/j.issn.1003-9961.2015.05.007
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