Skip to main content

Research progress on human infection with avian influenza H7N9

Abstract

Since the first case of novel H7N9 infection was reported, China has experienced five epidemics of H7N9. During the fifth wave, a highly pathogenic H7N9 strain emerged. Meanwhile, the H7N9 virus continues to accumulate mutations, and its affinity for the human respiratory epithelial sialic acid 2–6 receptor has increased. Therefore, a pandemic is still possible. In the past 6 years, we have accumulated rich experience in dealing with H7N9, especially in terms of virus tracing, epidemiological research, key site mutation monitoring, critical disease mechanisms, clinical treatment, and vaccine development. In the research fields above, significant progress has been made to effectively control the spread of the epidemic and reduce the fatality rate. To fully document the research progress concerning H7N9, we reviewed the clinical and epidemiological characteristics of H7N9, the key gene mutations of the virus, and H7N9 vaccine, thus providing a scientific basis for further monitoring and prevention of H7N9 influenza epidemics.

References

  1. Liu T, Kang M, Zhang B, Xiao J, Lin H, Zhao Y, Huang Z, Wang X, Zhang Y, He J, Ma W. Independent and interactive effects of ambient temperature and absolute humidity on the risks of avian influenza A(H7N9) infection in China. Sci Total Environ 2018; 619–620: 1358–1365

    Article  CAS  Google Scholar 

  2. Skowronski DM, Chambers C, Gustafson R, Purych DB, Tang P, Bastien N, Krajden M, Li Y. Avian influenza A(H7N9) virus infection in 2 travelers returning from China to Canada, January 2015. Emerg Infect Dis 2016; 22(1): 71–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. William T, Thevarajah B, Lee SF, Suleiman M, Jeffree MS, Menon J, Saat Z, Thayan R, Tambyah PA, Yeo TW. Avian influenza (H7N9) virus infection in Chinese tourist in Malaysia, 2014. Emerg Infect Dis 2015; 21(1): 142–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, Wo J, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S, Diao H, Xia S, Zhang Y, Chan KH, Tsoi HW, Teng JL, Song W, Wang P, Lau SY, Zheng M, Chan JF, To KK, Chen H, Li L, Yuen KY. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 2013; 381(9881): 1916–1925

    Article  CAS  Google Scholar 

  5. Wang X, Jiang H, Wu P, Uyeki TM, Feng L, Lai S, Wang L, Huo X, Xu K, Chen E, Wang X, He J, Kang M, Zhang R, Zhang J, Wu J, Hu S, Zhang H, Liu X, Fu W, Ou J, Wu S, Qin Y, Zhang Z, Shi Y, Zhang J, Artois J, Fang VJ, Zhu H, Guan Y, Gilbert M, Horby PW, Leung GM, Gao GF, Cowling BJ, Yu H. Epidemiology of avian influenza A H7N9 virus in human beings across five epidemics in mainland China, 2013–17: an epidemiological study of laboratory-confirmed case series. Lancet Infect Dis 2017; 17(8): 822–832

    Article  PubMed  PubMed Central  Google Scholar 

  6. Zhang F, Bi Y, Wang J, Wong G, Shi W, Hu F, Yang Y, Yang L, Deng X, Jiang S, He X, Liu Y, Yin C, Zhong N, Gao GF. Human infections with recently-emerging highly pathogenic H7N9 avian influenza virus in China. J Infect 2017; 75(1): 71–75

    Article  Google Scholar 

  7. Yang L, Zhu W, Li X, Chen M, Wu J, Yu P, Qi S, Huang Y, Shi W, Dong J, Zhao X, Huang W, Li Z, Zeng X, Bo H, Chen T, Chen W, Liu J, Zhang Y, Liang Z, Shi W, Shu Y, Wang D. Genesis and spread of newly emerged highly pathogenic H7N9 avian viruses in mainland China. J Virol 2017; 91(23): e01277–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Qi W, Jia W, Liu D, Li J, Bi Y, Xie S, Li B, Hu T, Du Y, Xing L, Zhang J, Zhang F, Wei X, Eden JS, Li H, Tian H, Li W, Su G, Lao G, Xu C, Xu B, Liu W, Zhang G, Ren T, Holmes EC, Cui J, Shi W, Gao GF, Liao M. Emergence and adaptation of a novel highly pathogenic H7N9 influenza virus in birds and humans from a 2013 human-infecting low-pathogenic ancestor. J Virol 2018; 92(2): e00921–17

    PubMed  PubMed Central  Google Scholar 

  9. Iuliano AD, Jang Y, Jones J, Davis CT, Wentworth DE, Uyeki TM, Roguski K, Thompson MG, Gubareva L, Fry AM, Burns E, Trock S, Zhou S, Katz JM, Jernigan DB. Increase in human infections with avian influenza A(H7N9) virus during the fifth epidemic — China, October, 2016–February, 2017. MMWR Morb Mortal Wkly Rep 2017; 66(9): 254–255

    Article  PubMed  PubMed Central  Google Scholar 

  10. Shi J, Deng G, Ma S, Zeng X, Yin X, Li M, Zhang B, Cui P, Chen Y, Yang H, Wan X, Liu L, Chen P, Jiang Y, Guan Y, Liu J, Gu W, Han S, Song Y, Liang L, Qu Z, Hou Y, Wang X, Bao H, Tian G, Li Y, Jiang L, Li C, Chen H. Rapid evolution of H7N9 highly pathogenic viruses that emerged in China in 2017. Cell Host Microbe 2018; 24(4): 558–568.e7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Quan C, Shi W, Yang Y, Yang Y, Liu X, Xu W, Li H, Li J, Wang Q, Tong Z, Wong G, Zhang C, Ma S, Ma Z, Fu G, Zhang Z, Huang Y, Song H, Yang L, Liu WJ, Liu Y, Liu W, Gao GF, Bi Y. New threats from H7N9 influenza virus: spread and evolution of high- and low-pathogenicity variants with high genomic diversity in Wave Five. J Virol 2018; 92(11): e00301–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gao HN, Lu HZ, Cao B, Du B, Shang H, Gan JH, Lu SH, Yang YD, Fang Q, Shen YZ, Xi XM, Gu Q, Zhou XM, Qu HP, Yan Z, Li FM, Zhao W, Gao ZC, Wang GF, Ruan LX, Wang WH, Ye J, Cao HF, Li XW, Zhang WH, Fang XC, He J, Liang WF, Xie J, Zeng M, Wu XZ, Li J, Xia Q, Jin ZC, Chen Q, Tang C, Zhang ZY, Hou BM, Feng ZX, Sheng JF, Zhong NS, Li LJ. Clinical findings in 111 cases of influenza A (H7N9) virus infection. N Engl J Med 2013; 368(24): 2277–2285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sun HY, Tong JH, Cui DW, Chen Y. Research progress on human infection with avian influenza H7N9. Chin J Clin Infect Dis (Zhonghua Lin Chuang Gan Ran Bing Za Zhi) 2017; 10(7): 8 (in Chinese)

    Google Scholar 

  14. State Health and Family Planning Commission of the People’s Republic of China. Diagnosis and treatment Program for Human infection with H7N9 Avian Influenza (2014 Edition). 2014

  15. Yang MF. Clinical study on the early warning of the severe avian influenza H7N9. Doctor Thesis. Zhejiang University School of Medicine, Hangzhou, Zhejiang, China, 2015 (in Chinese)

    Google Scholar 

  16. Jin C, Wu N, Peng X, Yao H, Lu X, Chen Y, Wu H, Xie T, Cheng L, Liu F, Kang K, Tang S, Li L. Comparison of a new gold immunochromatographic assay for the rapid diagnosis of the novel influenza A (H7N9) virus with cell culture and a real-time reverse-transcription PCR assay. BioMed Res Int 2014; 2014: 425051

    PubMed  PubMed Central  Google Scholar 

  17. Yu L, Wang Z, Chen Y, Ding W, Jia H, Chan JF, To KK, Chen H, Yang Y, Liang W, Zheng S, Yao H, Yang S, Cao H, Dai X, Zhao H, Li J, Bao Q, Chen P, Hou X, Li L, Yuen KY. Clinical, virological, and histopathological manifestations of fatal human infections by avian influenza A (H7N9) virus. Clin Infect Dis 2013; 57(10): 1449–1457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hu Y, Lu S, Song Z, Wang W, Hao P, Li J, Zhang X, Yen HL, Shi B, Li T, Guan W, Xu L, Liu Y, Wang S, Zhang X, Tian D, Zhu Z, He J, Huang K, Chen H, Zheng L, Li X, Ping J, Kang B, Xi X, Zha L, Li Y, Zhang Z, Peiris M, Yuan Z. Association between adverse clinical outcome in human disease caused by novel influenza A H7N9 virus and sustained viral shedding and emergence of antiviral resistance. Lancet 2013; 381(9885): 2273–2279

    Article  PubMed  PubMed Central  Google Scholar 

  19. Chen C, Chen J, Huang JA. Persistence of lymphocytopenia with CT abnormalities among patients with critical H7N9 swine-origin influenza A virus infection. Jpn J Radiol 2015; 33(10): 657–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Huang JB, Li HY, Liu JF, Lan CQ, Lin QH, Chen SX, Zhang HY, Wang XH, Lin X, Pan JG, Weng H. Histopathological findings in a critically ill patient with avian influenza A (H7N9). J Thorac Dis 2015; 7(12): E672–E677

    PubMed  PubMed Central  Google Scholar 

  21. Tsai NW, Ngai CW, Mok KL, Tsung JW. Lung ultrasound imaging in avian influenza A (H7N9) respiratory failure. Crit Ultrasound J 2014; 6(1): 6

    Article  PubMed  PubMed Central  Google Scholar 

  22. Yu H, Wu JT, Cowling BJ, Liao Q, Fang VJ, Zhou S, Wu P, Zhou H, Lau EH, Guo D, Ni MY, Peng Z, Feng L, Jiang H, Luo H, Li Q, Feng Z, Wang Y, Yang W, Leung GM. Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study. Lancet 2014; 383 (9916): 541–548

    Article  PubMed  PubMed Central  Google Scholar 

  23. Wang J, Su N, Dong Z, Liu C, Cui P, Huang JA, Chen C, Zhu Y, Chen L. The fifth influenza A (H7N9) epidemic: a family cluster of infection in Suzhou City of China, 2016. Int J Infect Dis 2018; 74: 128–135

    Article  PubMed  PubMed Central  Google Scholar 

  24. Liu S, Sun J, Cai J, Miao Z, Lu M, Qin S, Wang X, Lv H, Yu Z, Amer S, Chai C. Epidemiological, clinical and viral characteristics of fatal cases of human avian influenza A (H7N9) virus in Zhejiang Province, China. J Infect 2013; 67(6): 595–605

    Article  PubMed  PubMed Central  Google Scholar 

  25. Zheng S, Tang L, Gao H, Wang Y, Yu F, Cui D, Xie G, Yang X, Zhang W, Ye X, Zhang Z, Wang X, Yu L, Zhang Y, Yang S, Liang W, Chen Y, Li L. Benefit of early initiation of neuraminidase inhibitor treatment to hospitalized patients with avian influenza A (H7N9) virus. Clin Infect Dis 2018; 66(7): 1054–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhang Y, Gao H, Liang W, Tang L, Yang Y, Wu X, Yu L, Chen P, Zheng S, Ou H, Li L. Efficacy of oseltamivir-peramivir combination therapy compared to oseltamivir monotherapy for influenza A (H7N9) infection: a retrospective study. BMC Infect Dis 2016; 16 (1): 76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Xi ZQ, Zhou XM, Wang X, Bing QL, Chang N, Guo T, Zhong J, Feng GZ, Huang XM. Severe analysis of human H7N9 avian influenza treated with traditional Chinese medicine. Jiangsu J Tradit Chin Med (Jiangsu Zhong Yi Yao Za Zhi) 2015; 47(8): 13–17 (in Chinese)

    Google Scholar 

  28. Luo X, Shen X, Hu BX. Studies on the anti-influenza virus H7N9 of honeysuckle and Forsythia suspensa based on molecular docking method. Modern Tradit Chin Med (Xian Dai Zhong Yi Yao) 2016; 36(2): 75–78 (in Chinese)

    CAS  Google Scholar 

  29. Liu X, Zhang Y, Xu X, Du W, Su K, Zhu C, Chen Y, Lei S, Zheng S, Jiang J, Yang S, Guo J, Shao L, Yang Q, Chen J, Li L. Evaluation of plasma exchange and continuous veno-venous hemofiltration for the treatment of severe avian influenza A (H7N9): a cohort study. Ther Apher Dial 2015; 19(2): 178–184

    Article  PubMed  PubMed Central  Google Scholar 

  30. Yu WQ, Ding MD, Dai GH, Gu CJ, Xue L, Chen Y, Zhou DM, Xian JC, Xu HT. Analysis of 15 cases of avian influenza virus (H7N9) infection. Chin J Tuberc Respir Dis (Zhonghua Jie He He Hu Xi Za Zhi) 2018; 41(7): 534–538 (in Chinese)

    CAS  Google Scholar 

  31. Huang L, Zhang W, Yang Y, Wu W, Lu W, Xue H, Zhao H, Wu Y, Shang J, Cai L, Liu L, Liu D, Wang Y, Cao B, Zhan Q, Wang C. Application of extracorporeal membrane oxygenation in patients with severe acute respiratory distress syndrome induced by avian influenza A (H7N9) viral pneumonia: national data from the Chinese multicentre collaboration. BMC Infect Dis 2018; 18(1): 23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Nie Q, Zhang DY, Wu WJ, Huang CL, Ni ZY. Extracorporeal membrane oxygenation for avian influenza A (H7N9) patient with acute respiratory distress syndrome: a case report and short literature review. BMC Pulm Med 2017; 17(1): 38

    Article  PubMed  PubMed Central  Google Scholar 

  33. Qian L, Zheng J, Xu H, Shi L, Li L. Extracorporeal membrane oxygenation treatment of a H7N9-caused respiratory failure patient with mechanical valves replacement history: a case report. Medicine (Baltimore) 2016; 95(40): e5052

    Article  Google Scholar 

  34. Wang G, Zhou Y, Gong S, Dong H, Wu G, Xiang X, Tang J. A pregnant woman with avian influenza A (H7N9) virus pneumonia and ARDS managed with extracorporeal membrane oxygenation. Southeast Asian J Trop Med Public Health 2015; 46(3): 444–448

    PubMed  PubMed Central  Google Scholar 

  35. Tang X, He H, Sun B, Wan J, Ban C, Zhang C, Wang S, Xia J, Li J, Liu Y, Cao B, Tong Z. ARDS associated with pneumonia caused by avian influenza A H7N9 virus treated with extracorporeal membrane oxygenation. Clin Respir J 2015; 9(3): 380–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Liu C, Li J, Sun W, Yang R, Lu W, Gao D, Wu D. Extracorporeal membrane oxygenation as rescue therapy for H7N9 influenza-associated acute respiratory distress syndrome. Chin Med J (Engl) 2014; 127(9): 1798

    Google Scholar 

  37. Xi X, Fang Q, Gu Q, Du B; China Critical Care Clinical Trial Group (CCCCTG). Avian influenza A (H7N9) infections: intensivists as virus hunters in the new century. J Crit Care 2013; 28(4): 528–530

    Article  PubMed  PubMed Central  Google Scholar 

  38. Yang M, Gao H, Chen J, Xu X, Tang L, Yang Y, Liang W, Yu L, Sheng J, Li L. Bacterial coinfection is associated with severity of avian influenza A (H7N9), and procalcitonin is a useful marker for early diagnosis. Diagn Microbiol Infect Dis 2016; 84(2): 165–169

    Article  CAS  Google Scholar 

  39. Qin N, Zheng B, Yao J, Guo L, Zuo J, Wu L, Zhou J, Liu L, Guo J, Ni S, Li A, Zhu Y, Liang W, Xiao Y, Ehrlich SD, Li L. Influence of H7N9 virus infection and associated treatment on human gut microbiota. Sci Rep 2015; 5(1): 14771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hu X, Zhang H, Lu H, Qian G, Lv L, Zhang C, Guo J, Jiang H, Zheng B, Yang F, Gu S, Chen Y, Bao Q, Yu L, Jiang X, Hu Q, Shi H, Gao H, Li L. The effect of probiotic treatment on patients infected with the H7N9 influenza virus. PLoS One 2016; 11(3): e0151976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lu H, Zhang C, Qian G, Hu X, Zhang H, Chen C, Liang W, Gao H, Yang Y, Li L. An analysis of microbiota-targeted therapies in patients with avian influenza virus subtype H7N9 infection. BMC Infect Dis 2014; 14(1): 359

    Article  PubMed  PubMed Central  Google Scholar 

  42. Wang Z, Zhang A, Wan Y, Liu X, Qiu C, Xi X, Ren Y, Wang J, Dong Y, Bao M, Li L, Zhou M, Yuan S, Sun J, Zhu Z, Chen L, Li Q, Zhang Z, Zhang X, Lu S, Doherty PC, Kedzierska K, Xu J. Early hypercytokinemia is associated with interferon-induced transmembrane protein-3 dysfunction and predictive of fatal H7N9 infection. Proc Natl Acad Sci USA 2014; 111(2): 769–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Guo J, Huang F, Liu J, Chen Y, Wang W, Cao B, Zou Z, Liu S, Pan J, Bao C, Zeng M, Xiao H, Gao H, Yang S, Zhao Y, Liu Q, Zhou H, Zhu J, Liu X, Liang W, Yang Y, Zheng S, Yang J, Diao H, Su K, Shao L, Cao H, Wu Y, Zhao M, Tan S, Li H, Xu X, Wang C, Zhang J, Wang L, Wang J, Xu J, Li D, Zhong N, Cao X, Gao GF, Li L, Jiang C. The serum profile of hypercytokinemia factors identified in H7N9-infected patients can predict fatal outcomes. Sci Rep 2015; 5 (1): 10942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Huang F, Guo J, Zou Z, Liu J, Cao B, Zhang S, Li H, Wang W, Sheng M, Liu S, Pan J, Bao C, Zeng M, Xiao H, Qian G, Hu X, Chen Y, Chen Y, Zhao Y, Liu Q, Zhou H, Zhu J, Gao H, Yang S, Liu X, Zheng S, Yang J, Diao H, Cao H, Wu Y, Zhao M, Tan S, Guo D, Zhao X, Ye Y, Wu W, Xu Y, Penninger JM, Li D, Gao GF, Jiang C, Li L. Angiotensin II plasma levels are linked to disease severity and predict fatal outcomes in H7N9-infected patients. Nat Commun 2014; 5(1): 3595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Liu B, Havers FP, Zhou L, Zhong H, Wang X, Mao S, Li H, Ren R, Xiang N, Shu Y, Zhou S, Liu F, Chen E, Zhang Y, Widdowson MA, Li Q, Feng Z. Clusters of human infections with avian influenza A (H7N9) virus in China, March 2013 to June 2015. J Infect Dis 2017; 216(suppl_4): S548–S554

    Article  PubMed  PubMed Central  Google Scholar 

  46. Peiris JS, Cowling BJ, Wu JT, Feng L, Guan Y, Yu H, Leung GM. Interventions to reduce zoonotic and pandemic risks from avian influenza in Asia. Lancet Infect Dis 2016; 16(2): 252–258

    Article  PubMed  PubMed Central  Google Scholar 

  47. Gong Z, Lv H, Ding H, Han J, Sun J, Chai C, Cai J, Yu Z, Chen E. Epidemiology of the avian influenza A (H7N9) outbreak in Zhejiang Province, China. BMC Infect Dis 2014; 14(1): 244

    Article  PubMed  PubMed Central  Google Scholar 

  48. Chen E, Wang MH, He F, Sun R, Cheng W, Zee BCY, Lau SYF, Wang X, Chong KC. An increasing trend of rural infections of human influenza A (H7N9) from 2013 to 2017: a retrospective analysis of patient exposure histories in Zhejiang Province, China. PLoS One 2018; 13(2): e0193052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rogers GN, Daniels RS, Skehel JJ, Wiley DC, Wang XF, Higa HH, Paulson JC. Host-mediated selection of influenza virus receptor variants. Sialic acid-α 2,6Gal-specific clones of A/duck/Ukraine/1/63 revert to sialic acid-α 2,3Gal-specific wild type in ovo. J Biol Chem 1985; 260(12): 7362–7367

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Ou X, Chen F, Zhang R, Chen J, Liu R, Sun B. Analysis of the full-length genome of a novel strain of the H7N9 avian influenza virus. Exp Ther Med 2014; 7(5): 1369–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Liu Q, Zhou B, Ma W, Bawa B, Ma J, Wang W, Lang Y, Lyoo Y, Halpin RA, Lin X, Stockwell TB, Webby R, Wentworth DE, Richt JA. Analysis of recombinant H7N9 wild-type and mutant viruses in pigs shows that the Q226L mutation in HA is important for transmission. J Virol 2014; 88(14): 8153–8165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. de Vries RP, Peng W, Grant OC, Thompson AJ, Zhu X, Bouwman KM, de la Pena ATT, van Breemen MJ, Ambepitiya Wickramasinghe IN, de Haan CAM, Yu W, McBride R, Sanders RW, Woods RJ, Verheije MH, Wilson IA, Paulson JC. Three mutations switch H7N9 influenza to human-type receptor specificity. PLoS Pathog 2017; 13(6): e1006390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Wang D, Yang L, Gao R, Zhang X, Tan Y, Wu A, Zhu W, Zhou J, Zou S, Li X, Sun Y, Zhang Y, Liu Y, Liu T, Xiong Y, Xu J, Chen L, Weng Y, Qi X, Guo J, Li X, Dong J, Huang W, Zhang Y, Dong L, Zhao X, Liu L, Lu J, Lan Y, Wei H, Xin L, Chen Y, Xu C, Chen T, Zhu Y, Jiang T, Feng Z, Yang W, Wang Y, Zhu H, Guan Y, Gao GF, Li D, Han J, Wang S, Wu G, Shu Y. Genetic tuning of the novel avian influenza A(H7N9) virus during interspecies transmission, China, 2013. Euro Surveill 2014; 19(25): 20836

    Article  PubMed  PubMed Central  Google Scholar 

  54. Wan YH, Zhuang L, Zheng QN, Ren LJ, Fu L, Jiang WJ, Tang GP, Zhang DZ, Li SJ. Genetic characteristics of hemagglutinin and neuraminidase of avian influenza A (H7N9) virus in Guizhou Province, 2014–2017. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2018; 39(11): 1465–1471 (in Chinese)

    CAS  Google Scholar 

  55. Qi X, An X, Jiao Y, Yu H, Xu K, Cui L, Wang S, Deng F, Huo X, Huang H, Dai Q, Bao C. Co-circulation of multiple genotypes of influenza A (H7N9) viruses in eastern China, 2016–2017. Arch Virol 2018; 163(7): 1779–1793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Li J, Yu X, Pu X, Xie L, Sun Y, Xiao H, Wang F, Din H, Wu Y, Liu D, Zhao G, Liu J, Pan J. Environmental connections of novel avianorigin H7N9 influenza virus infection and virus adaptation to the human. Sci China Life Sci 2013; 56(6): 485–492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Wong CK, Zhu H, Li OT, Leung YH, Chan MC, Guan Y, Peiris JS, Poon LL. Molecular detection of human H7N9 influenza A virus causing outbreaks in China. Clin Chem 2013; 59(7): 1062–1067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ning T, Nie J, Huang W, Li C, Li X, Liu Q, Zhao H, Wang Y. Antigenic drift of influenza A (H7N9) virus hemagglutinin. J Infect Dis 2019; 219(1): 19–25

    Article  PubMed  PubMed Central  Google Scholar 

  59. Chang P, Sealy JE, Sadeyen JR, Iqbal M. Amino acid residue 217 in the hemagglutinin glycoprotein is a key mediator of avian influenza H7N9 virus antigenicity. J Virol 2018; 93(1): e01627–18

    Article  PubMed  PubMed Central  Google Scholar 

  60. Zou X, Guo Q, Zhang W, Chen H, Bai W, Lu B, Zhang W, Fan Y, Liu C, Wang Y, Zhou F, Cao B; Community-acquired Pneumonia-China Network. Dynamic variation and reversion in the signature amino acids of H7N9 virus during human infection. J Infect Dis 2018; 218(4): 586–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Dong Z, Xia Y, Ya X, Chen L, Liu C, Wang R, Shen Q. Epidemiological and genetic characteristics of the fifth avian influenza A (H7N9) wave in Suzhou, China, from October 2016 to April 2017. Virus Genes 2018; 54(2): 182–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Marjuki H, Mishin VP, Chesnokov AP, De La Cruz JA, Davis CT, Villanueva JM, Fry AM, Gubareva LV. Neuraminidase mutations conferring resistance to oseltamivir in influenza A(H7N9) viruses. J Virol 2015; 89(10): 5419–5426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Marjuki H, Mishin VP, Chesnokov AP, Jones J, De La Cruz JA, Sleeman K, Tamura D, Nguyen HT, Wu HS, Chang FY, Liu MT, Fry AM, Cox NJ, Villanueva JM, Davis CT, Gubareva LV. Characterization of drug-resistant influenza A (H7N9) variants isolated from an oseltamivir-treated patient in Taiwan. J Infect Dis 2015; 211(2): 249–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Yiu Lai K, Wing Yiu Ng G, Fai Wong K, Fan Ngai Hung I, Kam Fai Hong J, Fan Cheng F, Kwok Cheung Chan J. Human H7N9 avian influenza virus infection: a review and pandemic risk assessment. Emerg Microbes Infect 2013; 2(8): e48

    PubMed  PubMed Central  Google Scholar 

  65. Shi J, Deng G, Kong H, Gu C, Ma S, Yin X, Zeng X, Cui P, Chen Y, Yang H, Wan X, Wang X, Liu L, Chen P, Jiang Y, Liu J, Guan Y, Suzuki Y, Li M, Qu Z, Guan L, Zang J, Gu W, Han S, Song Y, Hu Y, Wang Z, Gu L, Yang W, Liang L, Bao H, Tian G, Li Y, Qiao C, Jiang L, Li C, Bu Z, Chen H. H7N9 virulent mutants detected in chickens in China pose an increased threat to humans. Cell Res 2017; 27(12): 1409–1421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Li W, Lee HHY, Li RF, Zhu HM, Yi G, Peiris JSM, Yang ZF, Mok CKP. The PB2 mutation with lysine at 627 enhances the pathogenicity of avian influenza (H7N9) virus which belongs to a non-zoonotic lineage. Sci Rep 2017; 7(1): 2352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Chen GW, Kuo SM, Yang SL, Gong YN, Hsiao MR, Liu YC, Shih SR, Tsao KC. Genomic signatures for avian H7N9 viruses adapting to humans. PLoS One 2016; 11(2): e0148432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Chan LL, Bui CT, Mok CK, Ng MM, Nicholls JM, Peiris JS, Chan MC, Chan RW. Evaluation of the human adaptation of influenza A/H7N9 virus in PB2 protein using human and swine respiratory tract explant cultures. Sci Rep 2016; 6(1): 35401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Mok CK, Lee HH, Lestra M, Nicholls JM, Chan MC, Sia SF, Zhu H, Poon LL, Guan Y, Peiris JS. Amino acid substitutions in polymerase basic protein 2 gene contribute to the pathogenicity of the novel A/H7N9 influenza virus in mammalian hosts. J Virol 2014; 88(6): 3568–3576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Deng Y, Li C, Han J, Wen Y, Wang J, Hong W, Li X, Liu Z, Ye Q, Li J, Zhou C, Yu L, Qin C, Zhang F, Jiang T. Phylogenetic and genetic characterization of a 2017 clinical isolate of H7N9 virus in Guangzhou, China during the fifth epidemic wave. Sci China Life Sci 2017; 60(12): 1331–1339

    Article  CAS  Google Scholar 

  71. Fries LF, Smith GE, Glenn GM. A recombinant viruslike particle influenza A (H7N9) vaccine. N Engl J Med 2013; 369(26): 2564–2566

    Article  CAS  Google Scholar 

  72. Bart SA, Hohenboken M, Della Cioppa G, Narasimhan V, Dormitzer PR, Kanesa-Thasan N. A cell culture-derived MF59-adjuvanted pandemic A/H7N9 vaccine is immunogenic in adults. Sci Transl Med 2014; 6(234): 234ra55

    Article  CAS  Google Scholar 

  73. Mulligan MJ, Bernstein DI, Winokur P, Rupp R, Anderson E, Rouphael N, Dickey M, Stapleton JT, Edupuganti S, Spearman P, Ince D, Noah DL, Hill H, Bellamy AR; DMID 13-0032 H7N9 Vaccine Study Group. Serological responses to an avian influenza A/H7N9 vaccine mixed at the point-of-use with MF59 adjuvant: a randomized clinical trial. JAMA 2014; 312(14): 1409–1419

    Article  CAS  Google Scholar 

  74. Jackson LA, Campbell JD, Frey SE, Edwards KM, Keitel WA, Kotloff KL, Berry AA, Graham I, Atmar RL, Creech CB, Thomsen IP, Patel SM, Gutierrez AF, Anderson EL, El Sahly HM, Hill H, Noah DL, Bellamy AR. Effect of varying doses of a monovalent H7N9 influenza vaccine with and without AS03 and MF59 adjuvants on immune response: a randomized clinical trial. JAMA 2015; 314(3): 237–246

    Article  CAS  Google Scholar 

  75. Madan A, Segall N, Ferguson M, Frenette L, Kroll R, Friel D, Soni J, Li P, Innis BL, Schuind A. Immunogenicity and safety of an AS03-adjuvanted H7N9 pandemic influenza vaccine in a randomized trial in healthy adults. J Infect Dis 2016; 214(11): 1717–1727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Rudenko L, Isakova-Sivak I, Naykhin A, Kiseleva I, Stukova M, Erofeeva M, Korenkov D, Matyushenko V, Sparrow E, Kieny MP. H7N9 live attenuated influenza vaccine in healthy adults: a randomised, double-blind, placebo-controlled, phase 1 trial. Lancet Infect Dis 2016; 16(3): 303–310

    Article  CAS  Google Scholar 

  77. Wu UI, Hsieh SM, Lee WS, Wang NC, Kung HC, Ou TY, Chen FL, Lin TY, Chen YC, Chang SC. Safety and immunogenicity of an inactivated cell culture-derived H7N9 influenza vaccine in healthy adults: a phase I/II, prospective, randomized, open-label trial. Vaccine 2017; 35(33): 4099–4104

    Article  CAS  Google Scholar 

  78. Wu J, Ke C, Lau EHY, Song Y, Cheng KL, Zou L, Kang M, Song T, Peiris M, Yen HL. Influenza H5/H7 virus vaccination in poultry and reduction of zoonotic infections, Guangdong Province, China, 2017–18. Emerg Infect Dis 2019; 25(1): 116–118

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the State Project of Essential Drug Research and Development (No. 2015ZX09101044).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lanjuan Li.

Ethics declarations

Xiaoxin Wu, Lanlan Xiao, and Lanjuan Li declare that they have no financial conflicts of interest. This manuscript is a review article and does not require approval by a relevant institutional review board or ethics committee.

Electronic supplementary material

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.

The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wu, X., Xiao, L. & Li, L. Research progress on human infection with avian influenza H7N9. Front. Med. 14, 8–20 (2020). https://doi.org/10.1007/s11684-020-0739-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11684-020-0739-z

Keywords

  • H7N9
  • pandemic
  • epidemiology
  • mutations
  • vaccine
  • influenza