Effectiveness of Live Poultry Market Interventions on Human Infection with Avian Influenza A(H7N9) Virus, China
Wei Wang
1, Jean Artois
1, Xiling Wang, Adam J. Kucharski, Yao Pei, Xin Tong, Victor Virlogeux, Peng Wu, Benjamin J. Cowling, Marius Gilbert
2, and Hongjie Yu
2
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
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).
Main Article
References
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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed Friedrich MJ.
Closing live poultry markets slowed avian flu in China. JAMA.
2013;
310:
2497.
DOI 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.
PubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOI 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed Shaman J,
Kohn M.
Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A.
2009;
106:
3243–
8.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
DOIPubMed 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.
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.
DOIPubMed
Main Article
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.