Interventions in live poultry markets for the control of avian influenza: A systematic review

One Health

Volumn 2, Issue , 2016, Pages 55-64

  Offeddu, Vittoria ^a   Cowling, Benjamin J ^a   Peiris, J S Malik ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

A H7N9; A H9N2; Closure; Influenza A virus; Live poultry market; Rest day

Indexed keywords

AVIAN INFLUENZA; DISINFECTION; HUMAN; HYGIENE; INCIDENCE; INFECTION; LIVE POULTRY MARKET; MARKET; REVIEW; RISK ASSESSMENT; RISK FACTOR; RISK REDUCTION; SYSTEMATIC REVIEW; VIRUS REPLICATION; VIRUS TRANSMISSION;

EID: 84962699151     PISSN: None     EISSN: 23527714     Source Type: Journal    
DOI: 10.1016/j.onehlt.2016.03.002     Document Type: Review

References (52)

1. World Health Organization Influenza 2015, URL:, accessed: 28.09.2015. http://www.who.int/topics/influenza/en/.
2. Yoon S.W., Webby R.J., Webster R.G. Evolution and ecology of influenza A viruses. Curr. Top. Microbiol. Immunol. 2014, 385:359-375.
3. Yiu Lai K., Wing Yiu Ng G., Fai Wong K., Fan Ngai Hung I., Kam Fai Hong J., et al. Human H7N9 avian influenza virus infection: a review and pandemic risk assessment. Emerg. Microbes Infect. 2013, 2.
4. Guan Y., Smith G.J. The emergence and diversification of panzootic H5N1 influenza viruses. Virus Res. 2013, 178:35-43.
5. Poovorawan Y., Pyungporn S., Prachayangprecha S., Makkoch J. Global alert to avian influenza virus infection: from H5N1 to H7N9. Pathog. Glob. Health 2013, 107:217-223.
6. Guan Y., Vijaykrishna D., Bahl J., Zhu H., Wang J., et al. The emergence of pandemic influenza viruses. Protein Cell 2010, 1:9-13.
7. Kageyama S. Pandemic influenza: a never-ending story. Yonago Acta Med. 2011, 54:41-48.
8. Peiris M., Yen H.L. Animal and human influenzas. Rev. Sci. Tech. 2014, 33:539-553.
9. Webster R.G. Wet markets-a continuing source of severe acute respiratory syndrome and influenza?. Lancet 2004, 363:234-236.
10. Hatta M., Kawaoka Y. The continued pandemic threat posed by avian influenza viruses in Hong Kong. Trends Microbiol. 2002, 10:340-344.
11. Sims L.D., Peiris M. One health: the Hong Kong experience with avian influenza. Curr. Top. Microbiol. Immunol. 2013, 365:281-298.
12. Fournie G., Pfeiffer D.U. Can closure of live poultry markets halt the spread of H7N9?. Lancet 2014, 383:496-497.
13. Nguyen D.C., Uyeki T.M., Jadhao S., Maines T., Shaw M., et al. Isolation and characterization of avian influenza viruses, including highly pathogenic H5N1, from poultry in live bird markets in Hanoi, Vietnam, in 2001. J. Virol. 2005, 79:4201-4212.
14. Chen H., Smith G.J., Li K.S., Wang J., Fan X.H., et al. Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2845-2850.
15. Guan Y., Chen H., Li K., Riley S., Leung G., et al. A model to control the epidemic of H5N1 influenza at the source. BMC Infect. Dis. 2007, 7:132.
16. Heymann D.L., Dixon M. Infections at the animal/human interface: shifting the paradigm from emergency response to prevention at source. Curr. Top. Microbiol. Immunol. 2013, 366:207-215.
17. Yuan J., Liao Q., Xie C.J., Ma X.W., Cai W.F., et al. Attitudinal changes toward control measures in live poultry markets among the general public and live poultry traders, Guangzhou, China, January-February, 2014. Am. J. Infect. Control 2014, 42:1322-1324.
18. He Y., Liu P., Tang S., Chen Y., Pei E., et al. Live poultry market closure and control of avian influenza A(H7N9), Shanghai, China. Emerg. Infect. Dis. 2014, 20:1565-1566.
19. Kung N.Y., Guan Y., Perkins N.R., Bissett L., Ellis T., et al. The impact of a monthly rest day on avian influenza virus isolation rates in retail live poultry markets in Hong Kong. Avian Dis. 2003, 47:1037-1041.
20. Lau E.H., Leung Y.H., Zhang L.J., Cowling B.J., Mak S.P., et al. Effect of interventions on influenza A (H9N2) isolation in Hong Kong's live poultry markets, 1999-2005. Emerg. Infect. Dis. 2007, 13:1340-1347.
21. Leung Y.H., Lau E.H., Zhang L.J., Guan Y., Cowling B.J., et al. Avian influenza and ban on overnight poultry storage in live poultry markets, Hong Kong. Emerg. Infect. Dis. 2012, 18:1339-1341.
22. Mullaney R. Live-bird market closure activities in the northeastern United States. Avian Dis. 2003, 47:1096-1098.
23. Trock S.C., Gaeta M., Gonzalez A., Pederson J.C., Senne D.A. Evaluation of routine depopulation, cleaning, and disinfection procedures in the live bird markets, New York. Avian Dis. 2008, 52:160-162.
24. Trock S.C., Huntley J.P. Surveillance and control of avian influenza in the New York live bird markets. Avian Dis. 2010, 54:340-344.
25. Centers for Disease Control and Prevention (CDC) Emergence of avian influenza A(H7N9) virus causing severe human illness - China, February-April 2013. MMWR Morb. Mortal. Wkly Rep. 2013, 62:366-371.
26. 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, 58:1037-1038.
27. Kang M., He J., Song T., Rutherford S., Wu J., et al. Environmental sampling for Avian Influenza A(H7N9) in Live-Poultry Markets in Guangdong, China. PLoS One 2015, 10.
28. Chowell G., Simonsen L., Towers S., Miller M.A., Viboud C. Transmission potential of influenza A/H7N9, February to May 2013, China. BMC Med. 2013, 11:214.
29. Yu H., Wu J.T., Cowling B.J., Liao Q., Fang V.J., 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, 383:541-548.
30. Lau E.H., Zheng J., Tsang T.K., Liao Q., Lewis B., et al. Accuracy of epidemiological inferences based on publicly available information: retrospective comparative analysis of line lists of human cases infected with influenza A(H7N9) in China. BMC Med. 2014, 12:88.
31. Wu P., Jiang H., Wu J.T., Chen E., He J., et al. Poultry market closures and human infection with influenza A(H7N9) virus, China, 2013-14. Emerg. Infect. Dis. 2014, 20:1891-1894.
32. Kucharski A.J., Mills H.L., Donnelly C.A., Riley S. Transmission potential of influenza A (H7N9) virus, China, 2013-2014. Emerg. Infect. Dis. 2015, 21:852-855.
33. Murhekar M., Arima Y., Horby P., Vandemaele K.A., Vong S., et al. Avian influenza A(H7N9) and the closure of live bird markets. Western Pac. Surveill. Response J.: WPSAR 2013, 4:4-7.
34. Han J., Jin M., Zhang P., Liu J., Wang L., et al. Epidemiological link between exposure to poultry and all influenza A(H7N9) confirmed cases in Huzhou city, China, March to May 2013. Euro Surveill. 2013, 18.
35. Xiang N., Havers F., Chen T., Song Y., Tu W., et al. Use of national pneumonia surveillance to describe influenza A(H7N9) virus epidemiology, China, 2004-2013. Emerg. Infect. Dis. 2013, 19:1784-1790.
36. Pepin K.M., Lloyd-Smith J.O., Webb C.T., Holcomb K., Zhu H., et al. Minimizing the threat of pandemic emergence from avian influenza in poultry systems. BMC Infect. Dis. 2013, 13:592.
37. FAO Biosecurity guide for live poultry markets 2015, Food and Agriculture Organization of the United Nations, Rome.
38. Fielding R., Leung G.M., Lam W.W., Jiang C.Q., Sitthi-Amorn C., et al. A pan-Asian survey of risk perception, attitudes and practices associated with live animal markets. Hong Kong Med. J. 2009, 15(Suppl. 6):17-20.
39. Ma X., Liao Q., Yuan J., Liu Y., Chen J., et al. Knowledge, attitudes and practices relating to influenza A(H7N9) risk among live poultry traders in Guangzhou City, China. BMC Infect. Dis. 2014, 14:554.
40. Li Q., Zhou L., Zhou M., Chen Z., Li F., et al. Epidemiology of human infections with avian influenza A(H7N9) virus in China. N. Engl. J. Med. 2014, 370:520-532.
41. Cowling B.J., Jin L., Lau E.H., Liao Q., Wu P., 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.
42. Shaman J., Kohn M. Absolute humidity modulates influenza survival, transmission, and seasonality. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3243-3248.
43. Park A.W., Glass K. Dynamic patterns of avian and human influenza in east and southeast Asia. Lancet Infect. Dis. 2007, 7:543-548.
44. Qi X., Cui L., Yu H., Ge Y., Tang F. Whole-genome sequence of a reassortant H5N6 avian influenza virus isolated from a live poultry market in China. Genome Announc. 2014, 2013:2.
45. Yuan J., Zhang L., Kan X., Jiang L., Yang J., et al. Origin and molecular characteristics of a novel 2013 avian influenza A(H6N1) virus causing human infection in Taiwan. Clin. Infect. Dis. 2013, 57:1367-1368.
46. World Health Organization Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness URL:, (accessed: 28.09.2015). http://www.who.int/influenza/vaccines/virus/characteristics_virus_vaccines/en/.
47. Cox N.J., Trock S.C., Burke S.A. Pandemic preparedness and the Influenza Risk Assessment Tool (IRAT). Curr. Top. Microbiol. Immunol. 2014, 385:119-136.
48. Qi X., Jiang D., Wang H., Zhuang D., Ma J., et al. Calculating the burden of disease of avian-origin H7N9 infections in China. BMJ Open 2014, 4.
49. FAO Addressing Avian Influenza A(H7N9). Qualitative Risk Assessment Update 2014, Food and Agriculture Organization of the United Nations, (URL: http://www.fao.org/docrep/019/i3631e/i3631e.pdf (accessed: 28.09.2015)).
50. Ai J., Huang Y., Xu K., Ren D., Qi X., et al. Case-control study of risk factors for human infection with influenza A(H7N9) virus in Jiangsu Province, China, 2013. Euro Surveill. 2013, 18:20510.
51. Liu B., Havers F., Chen E., Yuan Z., Yuan H., et al. Risk factors for influenza A(H7N9) disease-China, 2013. Clin. Infect. Dis. 2014, 59:787-794.
52. Li J., Chen J., Yang G., Zheng Y.X., Mao S.H., et al. Case-control study of risk factors for human infection with avian influenza A(H7N9) virus in Shanghai, China, 2013. Epidemiol. Infect. 2015, 143:1826-1832.