Skip directly to page options Skip directly to A-Z link

Volume 26, Number 5—May 2020

Research

Effectiveness of Live Poultry Market Interventions on Human Infection with Avian Influenza A(H7N9) Virus, China

Wei Wang1, Jean Artois1, Xiling Wang, Adam J. Kucharski, Yao Pei, Xin Tong, Victor Virlogeux, Peng Wu, Benjamin J. Cowling, Marius Gilbert2, and Hongjie Yu2Comments to Author 
Author affiliations: Fudan University School of Public Health, Shanghai, China (W. Wang, X. Wang, Y. Pei, X. Tong, H. Yu); Université Libre de Bruxelles, Brussels, Belgium (J. Artois, M. Gilbert); London School of Hygiene and Tropical Medicine, London, UK (A.J. Kucharski); École Normale Supérieure de Lyon, Lyon, France (V. Virlogeux); Cancer Research Center of Lyon, Lyon (V. Virlogeux); School of Public Health, University of Hong Kong, Hong Kong, China (V. Virlogeux, P. Wu, B.J. Cowling); Fonds National de la Recherche Scientifique, Brussels (M. Gilbert)

Main Article

Figure 2

Estimated daily incidence rates in counties with various levels of live poultry market closures across waves of influenza A(H7N9) infections, by duration of closure, China, 2013–2017. A) Wave 1; B) wave 2; C) wave 3; D) wave 4; E) wave 5. Error bars indicate 95% CIs. Asterisks (*) above bars indicate statistically significant (p<0.05) differences between daily incidence rates and reference category (Ref.) rates. Duration categories: no closure during epidemic wave; permanent closure, permanen

Figure 2. Estimated daily incidence rates in counties with various levels of live poultry market closures across waves of influenza A(H7N9) infections, by duration of closure, China, 2013–2017. A) Wave 1; B) wave 2; C) wave 3; D) wave 4; E) wave 5. Error bars indicate 95% CIs. Asterisks (*) above bars indicate statistically significant (p<0.05) differences between daily incidence rates and reference category (Ref.) rates. Duration categories: no closure during epidemic wave; permanent closure, permanently closed within the epidemic wave or for the entire epidemic wave duration; long-period closure (>14 days within the epidemic wave [10,17]); short-period closure (<14 days within the epidemic wave); and recursive closure, whereby LPMs were closed for 1 or 2 day with a repetition of the closing over time (the closing might be implemented weekly, biweekly, or monthly).

Download

Main Article

References
  1. Liu  D, Shi  W, Shi  Y, Wang  D, Xiao  H, Li  W, et al. Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet. 2013;381:1926–32. DOIPubMedGoogle Scholar
  2. World Health Organization. Human infection with avian influenza A(H7N9) virus—China. 2019 [cited 2019 Nov 23]. https://www.who.int/csr/don/13-september-2017-ah7n9-china
  3. Zhou  L, Chen  E, Bao  C, Xiang  N, Wu  J, Wu  S, et al. Clusters of human infection and human-to-human transmission of avian influenza A(H7N9) virus, 2013–2017. Emerg Infect Dis. 2018;24:397–400. DOIPubMedGoogle Scholar
  4. Bertran  K, Balzli  C, Kwon  YK, Tumpey  TM, Clark  A, Swayne  DE. Airborne transmission of highly pathogenic influenza virus during processing of infected poultry. Emerg Infect Dis. 2017;23:1806–14. DOIPubMedGoogle Scholar
  5. Centers for Disease Control and Prevention. Mutations on H7N9 virus have been identified in H7N9 patients in China. 2017 [cited 2018 Apr 20]. http://www.chinacdc.cn/jkzt/crb/zl/rgrgzbxqlgg/rgrqlgyp/201702/t20170219_138185.html
  6. Qi  W, Jia  W, Liu  D, Li  J, Bi  Y, Xie  S, et al. 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:e00921-17. DOIPubMedGoogle Scholar
  7. Artois  J, Jiang  H, Wang  X, Qin  Y, Pearcy  M, Lai  S, et al. Changing geographic patterns and risk factors for avian influenza A(H7N9) infections in humans, China. Emerg Infect Dis. 2018;24:87–94. DOIPubMedGoogle Scholar
  8. Lam  TT, Wang  J, Shen  Y, Zhou  B, Duan  L, Cheung  CL, et al. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature. 2013;502:241–4. DOIPubMedGoogle Scholar
  9. Wang  X, Jiang  H, Wu  P, Uyeki  TM, Feng  L, Lai  S, et al. 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;17:822–32. DOIPubMedGoogle Scholar
  10. He  Y, Liu  P, Tang  S, Chen  Y, Pei  E, Zhao  B, et al. Live poultry market closure and control of avian influenza A(H7N9), Shanghai, China. Emerg Infect Dis. 2014;20:1565–6. DOIPubMedGoogle Scholar
  11. Friedrich  MJ. Closing live poultry markets slowed avian flu in China. JAMA. 2013;310:2497. DOIGoogle Scholar
  12. Liu  H, Chen  Z, Xiao  X, Lu  J, Di  B, Li  K, et al. [Effects of resting days on live poultry markets in controlling the avian influenza pollution]. Zhonghua Liu Xing Bing Xue Za Zhi. 2014;35:832–6.PubMedGoogle Scholar
  13. Kang  M, He  J, Song  T, Rutherford  S, Wu  J, Lin  J, et al. Environmental sampling for avian influenza A(H7N9) in live-poultry markets in Guangdong, China. PLoS One. 2015;10:e0126335. DOIPubMedGoogle Scholar
  14. Yuan  J, Lau  EH, Li  K, Leung  YH, Yang  Z, Xie  C, et al. Effect of live poultry market closure on avian influenza A(H7N9) virus activity in Guangzhou, China, 2014. Emerg Infect Dis. 2015;21:1784–93. DOIPubMedGoogle Scholar
  15. Cheng  W, Wang  X, Shen  Y, Yu  Z, Liu  S, Cai  J, et al. Comparison of the three waves of avian influenza A(H7N9) virus circulation since live poultry markets were permanently closed in the main urban areas in Zhejiang Province, July 2014-June 2017. Influenza Other Respir Viruses. 2018;12:259–66. DOIPubMedGoogle Scholar
  16. Yu  H, Cowling  BJ, Liao  Q, Fang  VF, Zhou  S, Wu  P, et al. Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study. Lancet 2014;383:541–8. DOIGoogle Scholar
  17. Kucharski  AJ, Mills  HL, Donnelly  CA, Riley  S. Transmission potential of influenza A(H7N9) virus, China, 2013–2014. Emerg Infect Dis. 2015;21:852–5. DOIPubMedGoogle Scholar
  18. Virlogeux  V, Feng  L, Tsang  TK, Jiang  H, Fang  VJ, Qin  Y, et al. Evaluation of animal-to-human and human-to-human transmission of influenza A (H7N9) virus in China, 2013-15. Sci Rep. 2018;8:552. DOIPubMedGoogle Scholar
  19. Li  J, Rao  Y, Sun  Q, Wu  X, Jin  J, Bi  Y, et al. Identification of climate factors related to human infection with avian influenza A H7N9 and H5N1 viruses in China. Sci Rep. 2015;5:18094. DOIPubMedGoogle Scholar
  20. Shaman  J, Kohn  M. Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A. 2009;106:3243–8. DOIPubMedGoogle Scholar
  21. Yuan  J, Tang  X, Yang  Z, Wang  M, Zheng  B. Enhanced disinfection and regular closure of wet markets reduced the risk of avian influenza A virus transmission. Clin Infect Dis. 2014;58:1037–8. DOIPubMedGoogle Scholar
  22. Soares Magalhães  RJ, Zhou  X, Jia  B, Guo  F, Pfeiffer  DU, Martin  V. Live poultry trade in Southern China provinces and HPAIV H5N1 infection in humans and poultry: the role of Chinese New Year festivities. PLoS One. 2012;7:e49712. DOIPubMedGoogle Scholar
  23. Hu  J, Zhu  Y, Zhao  B, Li  J, Liu  L, Gu  K, et al. Limited human-to-human transmission of avian influenza A(H7N9) virus, Shanghai, China, March to April 2013. Euro Surveill. 2014;19:20838. DOIPubMedGoogle Scholar
  24. Liao  Q, Yuan  J, Lau  EH, Chen  GY, Yang  ZC, Ma  XW, et al. Live bird exposure among the general public, Guangzhou, China, May 2013. PLoS One. 2015;10:e0143582. DOIPubMedGoogle Scholar
  25. Nicita  A. Avian influenza and the poultry trade. 2008 [cited 2020 Feb 20]. https://elibrary.worldbank.org/doi/abs/10.1596/1813-9450-4551
  26. Lau  EH, Leung  YH, Zhang  LJ, Cowling  BJ, Mak  SP, Guan  Y, et al. Effect of interventions on influenza A (H9N2) isolation in Hong Kong’s live poultry markets, 1999-2005. Emerg Infect Dis. 2007;13:1340–7. DOIPubMedGoogle Scholar
  27. Wu  P, Wang  L, Cowling  BJ, Yu  J, Fang  VJ, Li  F, et al. Live poultry exposure and public response to influenza A(H7N9) in urban and rural China during two epidemic waves in 2013–2014. PLoS One. 2015;10:e0137831. DOIPubMedGoogle Scholar
  28. Offeddu  V, Cowling  BJ, Malik Peiris  JS. Interventions in live poultry markets for the control of avian influenza: a systematic review. One Health. 2016;2:55–64. DOIPubMedGoogle Scholar
  29. Sims  LD. Intervention strategies to reduce the risk of zoonotic infection with avian influenza viruses: scientific basis, challenges and knowledge gaps. Influenza Other Respir Viruses. 2013;7(Suppl 2):15–25. DOIPubMedGoogle Scholar
  30. Shi  J, Deng  G, Ma  S, Zeng  X, Yin  X, Li  M, et al. Rapid evolution of H7N9 highly pathogenic viruses that emerged in China in 2017. Cell Host Microbe. 2018;24:558–68.e7.
  31. Chen  E, Wang  MH, He  F, Sun  R, Cheng  W, Zee  BCY, et al. 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:e0193052. DOIPubMedGoogle Scholar

Main Article

1These authors contributed equally to this article.

2These authors are joint senior authors.

Page created: April 16, 2020
Page updated: April 16, 2020
Page reviewed: April 16, 2020
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external