Comparative epidemiology of human fatal infections with novel, high (H5N6 and H5N1) and low (H7N9 and H9N2) pathogenicity avian influenza a viruses

International Journal of Environmental Research and Public Health

Volumn 14, Issue 3, 2017, Pages

  Wu, Zu Qun ^a   Zhang, Yi ^b   Zhao, Na ^c   Yu, Zhao ^d   Pan, Hao ^e   Chan, Ta Chien ^f   Zhang, Zhi Ruo ^g   Liu, She Lan ^d  

^a THE SECOND AFFILIATED HOSPITAL OF ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Jinxi Petrochemical Corp of CNPC   (China)

^c INSTITUTE OF ZOOLOGY   (China)

^d ZHEJIANG PROVINCIAL CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^e Shanghai Municipal Centre for Disease Control and Prevention   (China)

^f RESEARCH CENTER FOR HUMANITIES AND SOCIAL SCIENCES   (Taiwan)

^g SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Endemic infection; Horizontal transmission; Influenza virus; Seasonal incidence

Indexed keywords

AVIAN INFLUENZA; COMPARATIVE STUDY; EPIDEMIOLOGY; HEALTH RISK; INFECTIOUS DISEASE; MORTALITY; PATHOGENICITY; RISK FACTOR; SURVIVAL;

ADOLESCENT; ADULT; AGED; ARTICLE; CASE FATALITY RATE; CAUSE OF DEATH; CHILD; CHINA; COMORBIDITY; CONTROLLED STUDY; FEMALE; HUMAN; INCIDENCE; INFANT; INFLUENZA A; INFLUENZA A (H5N1); INFLUENZA A (H5N6); INFLUENZA A (H7N9); INFLUENZA A (H9N2); INFLUENZA A VIRUS; INFLUENZA A VIRUS (H5N1); INFLUENZA A VIRUS (H5N6); INFLUENZA A VIRUS (H7N9); INFLUENZA A VIRUS (H9N2); MAJOR CLINICAL STUDY; MALE; MORBIDITY; MORTALITY; NONHUMAN; POPULATION RESEARCH; POULTRY; RETROSPECTIVE STUDY; RISK FACTOR; VIRUS VIRULENCE; ANIMAL; BIRD; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MIDDLE AGED; PATHOGENICITY; SEASON; VIROLOGY; VIRULENCE; YOUNG ADULT;

AVES; AVIAN INFLUENZA VIRUS; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

ADOLESCENT; ANIMALS; BIRDS; FEMALE; HUMANS; INCIDENCE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MALE; MIDDLE AGED; RISK FACTORS; SEASONS; VIRULENCE; YOUNG ADULT;

EID: 85014570528     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph14030263     Document Type: Article

References (46)

1. Jernigan, D.B.; Cox, N.J. H7N9: Preparing for the unexpected in influenza. Annu. Rev. Med. 2015, 66, 361–371. [CrossRef] [PubMed]
2. Senne, D.A. Avian influenza in North and South America, 2002–2005. Avian. Dis. 2007, 51, 167–173. [CrossRef] [PubMed]
3. Spackman, E.; Swayne, D.E.; Suarez, D.L.; Senne, D.A.; Pedersen, J.C.; Killian, M.L.; Pasick, J.; Handel, K.; Pillai, S.P.; Lee, C.W.; et al. Characterization of low-pathogenicity H5N1 avian influenza viruses from North America. J. Virol. 2007, 81, 11612–11619. [CrossRef] [PubMed]
4. Cross, T.A.; Arsnoe, D.M.; Minnis, R.B.; King, D.T.; Swafford, S.; Pedersen, K.; Owen, J.C. Prevalence of avian paramyxovirus 1 and avian influenza virus in double-crested Cormorants (Phalacrocorax auritus) in eastern North America. J. Wildl. Dis 2013, 49, 965–977. [CrossRef] [PubMed]
5. Liu, S.; Sun, J.; Cai, J.; Miao, Z.; Lu, M.; Qin, S.; Wang, X.; Lv, H.; Yu, Z.; Amer, S.; et al. Epidemiological, clinical and viral characteristics of fatal cases of human avian influenza A (H7N9) virus in Zhejiang Province, China. J. Infect. 2013, 67, 595–605. [CrossRef] [PubMed]
6. Li, Q.; Zhou, L.; Zhou, M.; Chen, Z.; Li, F.; Wu, H.; Xiang, N.; Chen, E.; Tang, F.; Wang, D.; et al. Epidemiology of human infections with avian influenza A(H7N9) virus in China. N. Engl. J. Med. 2014, 370, 520–532. [CrossRef] [PubMed]
7. Flint, P.L.; Pearce, J.M.; Franson, J.C.; Derksen, D.V. Wild bird surveillance for highly pathogenic avian influenza H5 in North America. Virol. J. 2015, 12, 151. [CrossRef] [PubMed]
8. Cowling, B.J.; Jin, L.; Lau, E.H.; Liao, Q.; Wu, P.; Jiang, H.; Tsang, T.K.; Zheng, J.; Fang, V.J.; Chang, Z.; et al. Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: A population-based study of laboratory-confirmed cases. Lancet 2013, 382, 129–137. [CrossRef]
9. Liu, T.; Bi, Z.; Wang, X.; Li, Z.; Ding, S.; Bi, Z.; Wang, L.; Pei, Y.; Song, S.; Zhang, S.; et al. One family cluster of avian influenza A (H7N9) virus infection in Shandong, China. BMC Infect. Dis. 2014, 14, 98. [CrossRef] [PubMed]
10. Qin, Y.; Horby, P.W.; Tsang, T.K.; Chen, E.; Gao, L.; Ou, J.; Nguyen, T.H.; Duong, T.N.; Gasimov, V.; Feng, L.; et al. Differences in the Epidemiology of Human Cases of Avian Influenza A(H7N9) and A(H5N1) Viruses Infection. Clin. Infect. Dis. 2015, 61, 563–571. [CrossRef] [PubMed]
11. Zhang, Y.; Shen, Z.; Ma, C.; Jiang, C.; Feng, C.; Shanker, N.; Yang, P.; Sun, W.; Wang, Q. Cluster of human infections with avian influenza A (H7N9) cases: A temporal and spatial analysis. Int. J. Environ. Res. Public Health 2015, 12, 816–828. [CrossRef] [PubMed]
12. Farooqui, A.; Liu, W.; Zeng, T.; Liu, Y.; Zhang, L.; Khan, A.; Wu, X.; Wu, R.; Wu, S.; Huang, L.; et al. Probable Hospital Cluster of H7N9 Influenza Infection. N. Engl. J. Med. 2016, 374, 596–598. [CrossRef] [PubMed]
13. Zhang, T.; Bi, Y.; Tianm, H.; Li, X.; Liu, D.; Wu, Y.; Jin, T.; Wang, Y.; Chen, Q.; Chen, Z.; et al. Human infection with influenza virus A(H10N8) from live poultry markets, China, 2014. Emerg. Infect. Dis. 2014, 20, 2076–2079. [CrossRef] [PubMed]
14. Shen, H.; Wu, B.; Chen, Y.; Bi, Y.; Xie, Q. Influenza A(H5N6) Virus Reassortant, Southern China, 2014. Emerg. Infect. Dis. 2015, 21, 1261–1262. [CrossRef] [PubMed]
15. CDC. Influenza Type A Viruses. 2015. Available online: https://www.cdc.gov/flu/avianflu/influenza-a-virus-subtypes.htm (accessed on 9 February 2015).
16. Centers for Disease Control and Prevention (CDC). Estimates of deaths associated with seasonal influenza—United States, 1976–2007. MMWR Morb. Mortal. Wkly. Rep. 2010, 59, 1057–1062.
17. Liu, S.L.; Wang, J.; Yang, X.H.; Chen, J.; Huang, R.J.; Ruan, B.; He, H.X.; Wang, C.M.; Zhang, H.M.; Sun, Z.; et al. Pandemic influenza A(H1N1) 2009 virus in pregnancy. Rev. Med. Virol. 2013, 23, 3–14. [CrossRef] [PubMed]
18. Uyeki, T.M.; Chong, Y.H.; Katz, J.M.; Lim, W.; Ho, Y.Y.; Wang, S.S.; Tsang, T.H.; Au, W.W.; Chan, S.C.; Rowe, T.; et al. Lack of evidence for human-to-human transmission of avian influenza A (H9N2) viruses in Hong Kong, China 1999. Emerg. Infect. Dis. 2002, 8, 154–159. [CrossRef] [PubMed]
19. Wu, Z.Q.; Sha, J.P.; Yu, Z.; Zhao, N.; Cheng, W.; Chan, T.C.; Amer, S.; Zhang, Z.R.; Liu, S.L. Epidemiological and virological differences in human clustered and sporadic infections with avian influenza A H7N9. Int. J. Infect. Dis. 2016, 49, 9–17. [CrossRef] [PubMed]
20. Xiao, X.C.; Li, K.B.; Chen, Z.Q.; Di, B.; Yang, Z.C.; Yuan, J.; Luo, H.B.; Ye, S.L.; Liu, H.; Lu, J.Y.; et al. Transmission of avian influenza A(H7N9) virus from father to child: A report of limited person-to-person transmission, Guangzhou, China, January 2014. Euro. Surveill. 2014, 19, 25. [CrossRef]
21. Yu, H.; Shu, Y.; Hu, S.; Zhang, H.; Gao, Z.; Chen, H.; Dong, J.; Xu, C.; Zhang, Y.; Xiang, N.; et al. The first confirmed human case of avian influenza A (H5N1) in Mainland China. Lancet 2006, 367, 84. [CrossRef]
22. Gao, R.; Cao, B.; Hu, Y.; Feng, Z.; Wang, D.; Hu, W.; Chen, J.; Jie, Z.; Qiu, H.; Xu, K.; et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 2013, 368, 1888–1897. [CrossRef] [PubMed]
23. Yang, Z.F.; Mok, C.K.; Peiris, J.S.; Zhong, N.S. Human Infection with a Novel Avian Influenza A (H5N6) Virus. N. Engl. J. Med. 2015, 373, 487–489. [CrossRef] [PubMed]
24. Liu, B.; Havers, F.; Chen, E.; Yuan, Z.; Yuan, H.; Ou, J.; Shang, M.; Kang, K.; Liao, K.; Liu, F.; et al. Risk factors for influenza A(H7N9) disease—China, 2013. Clin. Infect. Dis. 2014, 59, 787–794. [CrossRef] [PubMed]
25. Feikin, D.R.; Alraddadi, B.; Qutub, M.; Shabouni, O.; Curns, A.; Oboho, I.K.; Tomczyk, S.M.; Wolff, B.; Watson, J.T.; Madani, T.A. Association of Higher MERS-CoV Virus Load with Severe Disease and Death, Saudi Arabia, 2014. Emerg. Infect. Dis. 2015, 21, 2029–2035. [CrossRef] [PubMed]
26. Li, X.L.; Yang, Y.; Sun, Y.; Chen, W.J.; Sun, R.X.; Liu, K.; Ma, M.J.; Liang, S.; Yao, H.W.; Gray, G.C.; et al. Risk Distribution of Human Infections with Avian Influenza H7N9 and H5N1 virus in China. Sci. Rep. 2015, 5, 18610. [CrossRef] [PubMed]
27. Majumder, M.S.; Kluberg, S.A.; Mekaru, S.R.; Brownstein, J.S. Mortality Risk Factors for Middle East Respiratory Syndrome Outbreak, South Korea, 2015. Emerg. Infect. Dis. 2015, 21, 2088–2090. [CrossRef] [PubMed]
28. Alraddadi, B.M.; Watson, J.T.; Almarashi, A.; Abedi, G.R.; Turkistani, A.; Sadran, M.; Housa, A.; Almazroa, M.A.; Alraihan, N.; Banjar, A.; et al. Risk Factors for Primary Middle East Respiratory Syndrome Coronavirus Illness in Humans, Saudi Arabia, 2014. Emerg. Infect. Dis. 2016, 22, 49–55. [CrossRef] [PubMed]
29. Abdel-Ghafar, A.N.; Chotpitayasunondh, T.; Gao, Z.; Hayden, F.G.; Nguyen, D.H.; de Jong, M.D.; Naghdaliyev, A.; Peiris, J.S.; Shindo, N.; Soeroso, S.; et al. Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med. 2008, 358, 261–273. [PubMed]
30. Wang, X.; Fang, S.; Lu, X.; Xu, C.; Cowling, B.J.; Tang, X.; Peng, B.; Wu, W.; He, J.; Tang, Y.; et al. Seroprevalence to avian influenza A (H7N9) virus among poultry workers and the general population in southern China: A longitudinal study. Clin. Infect. Dis. 2014, 59, e76–83. [CrossRef] [PubMed]
31. Yang, S.; Chen, Y.; Cui, D.; Yao, H.; Lou, J.; Huo, Z.; Xie, G.; Yu, F.; Zheng, S.; Yang, Y.; et al. Avian-origin influenza A(H7N9) infection in influenza A(H7N9)-affected areas of China: a serological study. J. Infect. Dis. 2014, 209, 265–269. [CrossRef] [PubMed]
32. Yu, X.; Zhang, X.; He, Y.; Wu, H.; Gao, X.; Pan, Q.; Shen, J.; Zhu, J.; Chen, H.; Zhu, Y.; et al. Mild infection of a novel H7N9 avian influenza virus in children in Shanghai. Emerg. Microbes. Infect. 2013, 2, e41. [CrossRef] [PubMed]
33. Zeng, X.; Mai, W.; Shu, B.; Yi, L.; Lu, J.; Song, T.; Zhong, H.; Xiao, H.; Guan, D.; Wu, J.; et al. Mild influenza A/H7N9 infection among children in Guangdong Province. Pediatr. Infect. Dis. J. 2015, 34, 104–107. [CrossRef] [PubMed]
34. Ip, D.K.; Liao, Q.; Wu, P.; Gao, Z.; Cao, B.; Feng, L.; Xu, X.; Jiang, H.; Li, M.; Bao, J.; et al. Detection of mild to moderate influenza A/H7N9 infection by China’s national sentinel surveillance system for influenza-like illness: Case series. BMJ 2013, 346, f3693. [CrossRef] [PubMed]
35. Williams, J.V. The clinical presentation and outcomes of children infected with newly identified respiratory tract viruses. Infect. Dis. Clin. N. Am. 2005, 19, 569–584. [CrossRef] [PubMed]
36. Yu, H.; Cowling, B.J.; Feng, L.; Lau, E.H.; Liao, Q.; Tsang, T.K.; Peng, Z.; Wu, P.; Liu, F.; Fang, V.J.; et al. Human infection with avian influenza A H7N9 virus: An assessment of clinical severity. Lancet 2013, 382, 138–145. [CrossRef]
37. Simonsen, L.; Taylor, R.J.; Young-Xu, Y.; Haber, M.; May, L.; Klugman, K.P. Impact of pneumococcal conjugate vaccination of infants on pneumonia and influenza hospitalization and mortality in all age groups in the United States. MBio 2011, 2, e00309–e00310. [CrossRef] [PubMed]
38. Wu, P.; Peng, Z.; Fang, V.J.; Feng, L.; Tsang, T.K.; Jiang, H.; Lau, E.H.; Yang, J.; Zheng, J.; Qin, Y.; et al. Human Infection with Influenza A (H7N9) Virus during 3 Major Epidemic Waves, China, 2013–2015. Emerg. Infect. Dis. 2016, 22, 964–972. [CrossRef] [PubMed]
39. Chen, Y.; Liang, W.; Yang, S.; Wu, N.; Gao, H.; Sheng, J.; Yao, H.; Wo, J.; Fang, Q.; Cui, D.; et al. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 2013, 381, 1916–1925. [CrossRef]
40. Shen, Y.; Lu, H.; Qi, T.; Gu, Y.; Xiang, M.; Lu, S.; Qu, H.; Zhang, W.; He, J.; Cao, H.; et al. Fatal cases of human infection with avian influenza A (H7N9) virus in Shanghai, China in 2013. Biosci. Trends 2015, 9, 73–78. [CrossRef] [PubMed]
41. Adisasmito, W.; Chan, P.K.; Lee, N.; Oner, A.F.; Gasimov, V.; Aghayev, F.; Zaman, M.; Bamgboye, E.; Dogan, N.; Coker, R.; et al. Effectiveness of antiviral treatment in human influenza A(H5N1) infections: Analysis of a Global Patient Registry. J. Infect. Dis. 2010, 202, 1154–1160. [CrossRef] [PubMed]
42. Louie, J.K.; Yang, S.; Acosta, M.; Yen, C.; Samuel, M.C.; Schechter, R.; Guevara, H.; Uyeki, T.M. Treatment with neuraminidase inhibitors for critically ill patients with influenza A (H1N1)pdm09. Clin. Infect. Dis. 2012, 55, 1198–1204. [CrossRef] [PubMed]
43. Qi, X.; Qian, Y.H.; Bao, C.J.; Guo, X.L.; Cui, L.B.; Tang, F.Y.; Ji, H.; Huang, Y.; Cai, P.Q.; Lu, B.; et al. Probable person to person transmission of novel avian influenza A (H7N9) virus in Eastern China, 2013: Epidemiological investigation. BMJ 2013, 347, f4752. [CrossRef] [PubMed]
44. Ding, H.; Chen, Y.; Yu, Z.; Horby, P.W.; Wang, F.; Hu, J.; Yang, X.; Mao, H.; Qin, S.; Chai, C.; et al. A family cluster of three confirmed cases infected with avian influenza A (H7N9) virus in Zhejiang Province of China. BMC Infect. Dis. 2014, 14, 698. [CrossRef] [PubMed]
45. Gao, H.N.; Yao, H.P.; Liang, W.F.; Wu, X.X.; Wu, H.B.; Wu, N.P.; Yang, S.G.; Zhang, Q.; Su, K.K.; Guo, J.; et al. Viral genome and antiviral drug sensitivity analysis of two patients from a family cluster caused by the influenza A(H7N9) virus in Zhejiang, China, 2013. Int. J. Infect. Dis. 2014, 29, 254–258. [CrossRef] [PubMed]
46. Fang, C.F.; Ma, M.J.; Zhan, B.D.; Lai, S.M.; Hu, Y.; Yang, X.X.; Li, J.; Cao, G.P.; Zhou, J.J.; Zhang, J.M.; et al. Nosocomial transmission of avian influenza A (H7N9) virus in China: epidemiological investigation. BMJ 2015, 351, h5765. [CrossRef] [PubMed]