1921
Volume 97, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Almost all human infections by avian influenza viruses (AIVs) are transmitted from poultry. A systematic review was conducted to identify practices associated with human infections, their prevalence, and rationale. Observational studies were identified through database searches. Meta-analysis produced combined odds ratio estimates. The prevalence of practices and rationales for their adoptions were reported. Of the 48,217 records initially identified, 65 articles were included. Direct and indirect exposures to poultry were associated with infection for all investigated viral subtypes and settings. For the most frequently reported practices, association with infection seemed stronger in markets than households, for sick and dead than healthy poultry, and for H7N9 than H5N1. Practices were often described in general terms and their frequency and intensity of contact were not provided. The prevalence of practices was highly variable across studies, and no studies comprehensively explored reasons behind the adoption of practices. Combining epidemiological and targeted anthropological studies would increase the spectrum and detail of practices that could be investigated and should aim to provide insights into the rationale(s) for their existence. A better understanding of these rationales may help to design more realistic and acceptable preventive public health measures and messages.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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References

  1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y, , 1992. Evolution and ecology of influenza A viruses. Microbiol Rev 56: 152179. [Google Scholar]
  2. Kawaoka Y, Krauss S, Webster RG, , 1989. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol 63: 46034608. [Google Scholar]
  3. Smith GJ, , 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 11221125.[Crossref] [Google Scholar]
  4. Freidl GS, , 2014. Influenza at the animal-human interface: a review of the literature for virological evidence of human infection with swine or avian influenza viruses other than A(H5N1). Euro Surveill 19: 20793.[Crossref] [Google Scholar]
  5. Khan SU, Anderson BD, Heil GL, Liang S, Gray GC, , 2015. A systematic review and meta-analysis of the seroprevalence of influenza A(H9N2) infection among humans. J Infect Dis 212: 562569.[Crossref] [Google Scholar]
  6. World Health Organization (WHO), 2015. Cumulative Number of Confirmed Human Cases for Avian Influenza A(H5N1) Reported to WHO, 2003–2015. Available at: http://www.who.int/influenza/human_animal_interface/EN_GIP_20150717cumulativeNumberH5N1cases.pdf?ua=1. Accessed August 13, 2015. [Google Scholar]
  7. Li C, Hatta M, Nidom CA, Muramoto Y, Watanabe S, Neumann G, Kawaoka Y, , 2010. Reassortment between avian H5N1 and human H3N2 influenza viruses creates hybrid viruses with substantial virulence. Proc Natl Acad Sci USA 107: 46874692.[Crossref] [Google Scholar]
  8. Russell CA, , 2012. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336: 15411547.[Crossref] [Google Scholar]
  9. Rabinowitz P, Perdue M, Mumford E, , 2010. Contact variables for exposure to avian influenza H5N1 virus at the human-animal interface. Zoonoses Public Health 57: 227238.[Crossref] [Google Scholar]
  10. Van Kerkhove MD, Mumford E, Mounts AW, Bresee J, Ly S, Bridges CB, Otte J, , 2011. Highly pathogenic avian influenza (H5N1): pathways of exposure at the animal-human interface, a systematic review. PLoS One 6: e14582.[Crossref] [Google Scholar]
  11. Lai S, , 2016. Global epidemiology of avian influenza A H5N1 virus infection in humans, 1997–2015: a systematic review of individual case data. Lancet Infect Dis 16: e108e118.[Crossref] [Google Scholar]
  12. Costard S, Fournie G, Pfeiffer DU, , 2014. Using risk assessment as part of a systems approach to the control and prevention of HPAIV H5N1. EcoHealth 11: 3643.[Crossref] [Google Scholar]
  13. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P, , 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6: e1000097.[Crossref] [Google Scholar]
  14. Claas EC, Osterhaus AD, van Beek R, De Jong JC, Rimmelzwaan GF, Senne DA, Krauss S, Shortridge KF, Webster RG, , 1998. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351: 472477.[Crossref] [Google Scholar]
  15. Sterne JAC, Higgins JPT, Reeves BC, , 2014. A Cochrane Risk Of Bias Assessment Tool: for Non-Randomized Studies of Interventions (ACROBAT NRSI), Version 1.0.0. 24 September 2014 . Available at: sites.google.com/site/riskofbiastool/. Accessed February 1, 2016. [Google Scholar]
  16. Higgins JP, Thompson SG, Deeks JJ, Altman DG, , 2003. Measuring inconsistency in meta-analyses. BMJ 327: 557560.[Crossref] [Google Scholar]
  17. DerSimonian R, Laird N, , 1986. Meta-analysis in clinical trials. Control Clin Trials 7: 177188.[Crossref] [Google Scholar]
  18. R Development Core Team, 2015. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. [Google Scholar]
  19. Viechtbauer W, , 2010. Conducting meta-analyses in R with the metafor package. J Stat Software 36: 148.[Crossref] [Google Scholar]
  20. Mounts AW, , 1999. Case-control study of risk factors for avian influenza A (H5N1) disease, Hong Kong, 1997. J Infect Dis 180: 505508.[Crossref] [Google Scholar]
  21. Zhou L, , 2009. Risk factors for human illness with avian influenza A (H5N1) virus infection in China. J Infect Dis 199: 17261734.[Crossref] [Google Scholar]
  22. Areechokchai D, Jiraphongsa C, Laosiritaworn Y, Hanshaoworakul W, , O'Reilly M; Centers for Disease Control and Prevention, 2006. Investigation of avian influenza (H5N1) outbreak in humans–Thailand, 2004. MMWR Morb Mortal Wkly Rep 55: 36. [Google Scholar]
  23. Dinh PN, Long HT, Tien NT, Hien NT, Mai le TQ, Phong le H, Tuan le V, Van Tan H, Nguyen NB, Van Tu P, Phuong NT, , 2006. Risk factors for human infection with avian influenza A H5N1, Vietnam, 2004. Emerg Infect Dis 12: 18411847.[Crossref] [Google Scholar]
  24. Yupiana Y, de Vlas SJ, Adnan NM, Richardus JH, , 2010. Risk factors of poultry outbreaks and human cases of H5N1 avian influenza virus infection in West Java Province, Indonesia. Int J Infect Dis 14: e800e805.[Crossref] [Google Scholar]
  25. Vong S, Ly S, Van Kerkhove MD, Achenbach J, Holl D, Buchy P, Sorn S, Seng H, Uyeki TM, Sok T, Katz JM, , 2009. Risk factors associated with subclinical human infection with avian influenza A (H5N1) virus–Cambodia, 2006. J Infect Dis 199: 17441752.[Crossref] [Google Scholar]
  26. Bridges CB, , 2002. Risk of influenza A (H5N1) infection among poultry workers, Hong Kong, 1997–1998. J Infect Dis 185: 10051010.[Crossref] [Google Scholar]
  27. Cavailler P, Chu S, Ly S, Garcia JM, Ha do Q, Bergeri I, Som L, Sok T, Vong S, Buchy P, , 2010. Seroprevalence of anti-H5 antibody in rural Cambodia, 2007. J Clin Virol 48: 123126.[Crossref] [Google Scholar]
  28. Huo X, Zu RQ, Qi X, Qin YF, Li L, Tang FY, Hu ZB, Zhu FC, , 2012. Seroprevalence of avian influenza A (H5N1) virus among poultry workers in Jiangsu Province, China: an observational study. BMC Infect Dis 12: 93.[Crossref] [Google Scholar]
  29. Li LH, Yu Z, Chen WS, Liu SL, Lu Y, Zhang YJ, Chen EF, Lin JF, , 2013. Evidence for H5 avian influenza infection in Zhejiang province, China, 2010–2012: a cross-sectional study. J Thorac Dis 5: 790796.[Crossref] [Google Scholar]
  30. Gomaa MR, , 2015. Avian influenza A(H5N1) and A(H9N2) seroprevalence and risk factors for infection among Egyptians: a prospective, controlled seroepidemiological study. J Infect Dis 211: 13991407.[Crossref] [Google Scholar]
  31. Li J, Chen J, Yang G, Zheng YX, Mao SH, Zhu WP, Yu XL, Gao Y, Pan QC, Yuan ZA, , 2015. Case-control study of risk factors for human infection with avian influenza A (H7N9) virus in Shanghai, China, 2013. Epidemiol Infect 143: 18261832.[Crossref] [Google Scholar]
  32. Liu B, , 2014. Risk Factors for Influenza A(H7N9) Disease-China, 2013. Clin Infect Dis 59: 787794.[Crossref] [Google Scholar]
  33. He F, Zhang M, Wang XY, Wu HC, Shang XP, Li FD, Wu C, Lin JF, Zhu BP, , 2014. Distinct risk profiles for human infections with the influenza A(H7N9) virus among rural and urban residents: Zhejiang Province, China, 2013. PLoS One 9: e95015.[Crossref] [Google Scholar]
  34. Ai J, , 2013. Case-control study of risk factors for human infection with influenza A(H7N9) virus in Jiangsu Province, China, 2013. Euro Surveillance: Bulletin Europeen sur les Maladies Transmissibles 18: 20510. [Google Scholar]
  35. Yu H, , 2014. Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study. Lancet 383: 541548.[Crossref] [Google Scholar]
  36. Fang LQ, Li XL, Liu K, Li YJ, Yao HW, Liang S, Yang Y, Feng ZJ, Gray GC, Cao WC, , 2013. Mapping spread and risk of avian influenza A (H7N9) in China. Sci Rep 3: 2722.[Crossref] [Google Scholar]
  37. Fuller T, Havers F, Xu C, Fang LQ, Cao WC, Shu Y, Widdowson MA, Smith TB, , 2014. Identifying areas with a high risk of human infection with the avian influenza A (H7N9) virus in east Asia. J Infect 69: 174181.[Crossref] [Google Scholar]
  38. Wu P, , 2014. Poultry market closures and human infection with influenza A(H7N9) virus, China, 2013–14. Emerg Infect Dis 20: 18911894.[Crossref] [Google Scholar]
  39. Wang X, , 2014. Seroprevalence to avian influenza A(H7N9) virus among poultry workers and the general population in southern China: a longitudinal study. Clin Infect Dis 59: e76e83.[Crossref] [Google Scholar]
  40. Ahad A, , 2014. Risk factors for H7 and H9 infection in commercial poultry farm workers in provinces within Pakistan. Prev Vet Med 117: 610614.[Crossref] [Google Scholar]
  41. Yang P, , 2012. A serological survey of antibodies to H5, H7 and H9 avian influenza viruses amongst the duck-related workers in Beijing, China. PLoS One 7: e50770.[Crossref] [Google Scholar]
  42. Yu Q, , 2013. Risk perceptions for avian influenza virus infection among poultry workers, China. Emerg Infect Dis 19: 313316.[Crossref] [Google Scholar]
  43. Sultana R, Nahar N, Rimi NA, Azad S, Islam MS, Gurley ES, Luby SP, , 2012. Backyard poultry raising in Bangladesh: a valued resource for the villagers and a setting for zoonotic transmission of avian influenza. A qualitative study. Rural Remote Health 12: 1927. [Google Scholar]
  44. Sultana R, Rimi NA, Azad S, Islam MS, Khan MSU, Gurley ES, Nahar N, Luby SP, , 2012. Bangladeshi backyard poultry raisers' perceptions and practices related to zoonotic transmission of avian influenza. J Infect Dev Ctries 6: 156165.[Crossref] [Google Scholar]
  45. Edirne T, Avci DK, Dagkara B, Aslan M, , 2011. Knowledge and anticipated attitudes of the community about bird flu outbreak in Turkey, 2007–2008: a survey-based descriptive study. Int J Public Health 56: 163168.[Crossref] [Google Scholar]
  46. Ma X, , 2014. Knowledge, attitudes and practices relating to influenza A(H7N9) risk among live poultry traders in Guangzhou City, China. BMC Infect Dis 14: 554.[Crossref] [Google Scholar]
  47. Liao QY, Lam WWT, Bich TH, Dang VT, Fielding R, , 2014. Comparison of behaviors regarding live poultry exposure among rural residents in Vietnam and Thailand. J Infect Dev Ctries 8: 526534.[Crossref] [Google Scholar]
  48. Rimi NA, Sultana R, Ishtiak-Ahmed K, Khan SU, Sharker MAY, Uz Zaman R, Azziz-Baumgartner E, Gurley ES, Nahar N, Luby SP, , 2014. Poultry slaughtering practices in rural communities of Bangladesh and risk of avian influenza transmission: a qualitative study. EcoHealth 11: 8393.[Crossref] [Google Scholar]
  49. Negro-Calduch E, Elfadaly S, Tibbo M, Ankers P, Bailey E, , 2013. Assessment of biosecurity practices of small-scale broiler producers in central Egypt. Prev Vet Med 110: 253262.[Crossref] [Google Scholar]
  50. Barennes H, Harimanana AN, Lorvongseng S, Ongkhammy S, Chu C, , 2010. Paradoxical risk perception and behaviours related to Avian Flu outbreak and education campaign, Laos. BMC Infect Dis 10: 294.[Crossref] [Google Scholar]
  51. Barennes H, Martinez-Aussel B, Vongphrachanh P, Strobe M, , 2007. Avian influenza risk perceptions, Laos. Emerg Infect Dis 13: 11261128.[Crossref] [Google Scholar]
  52. Sutanto YC, , 2013. Highly Pathogenic Avian Influenza Knowledge, Attitudes, and Practices Study among Live Bird Market Workers in Jakarta—Indonesia. Fort Collins, CO: Department of Clinical Sciences, Colorado State University, 153. [Google Scholar]
  53. Shortridge KF, , 1998. Characterization of avian H5N1 influenza viruses from poultry in Hong Kong. Virology 252: 331342.[Crossref] [Google Scholar]
  54. Fournié G, Guitian J, Mangtani P, Ghani AC, , 2011. Impact of the implementation of rest days in live bird markets on the dynamics of H5N1 highly pathogenic avian influenza. J R Soc Interface 8: 10791089.[Crossref] [Google Scholar]
  55. Tellier R, , 2006. Review of aerosol transmission of influenza A virus. Emerg Infect Dis 12: 16571662.[Crossref] [Google Scholar]
  56. Webster RG, , 2002. Characterization of H5N1 influenza viruses that continue to circulate in geese in southeastern China. J Virol 76: 118126.[Crossref] [Google Scholar]
  57. Allen VM, Hinton MH, Tinker DB, Gibson C, Mead GC, Wathes CM, , 2003. Microbial cross-contamination by airborne dispersion and contagion during defeathering of poultry. Br Poult Sci 44: 567576.[Crossref] [Google Scholar]
  58. Offeddu V, Cowling BJ, Malik Peiris JS, , 2016. Interventions in live poultry markets for the control of avian influenza: a systematic review. One Health 2: 5564.[Crossref] [Google Scholar]
  59. Hill AB, , 1965. The environment and disease: association or causation? Proc R Soc Med 58: 295300. [Google Scholar]
  60. Lucas RM, McMichael AJ, , 2005. Association or causation: evaluating links between “environment and disease”. Bull World Health Organ 83: 792795. [Google Scholar]
  61. Aunger R, Curtis V, , 2015. Gaining Control: How Human Behavior Evolved. Oxford, United Kingdom: Oxford University Press.[Crossref] [Google Scholar]
  62. Barnett T, Fournie G, Gupta S, Seeley J, , 2015. Some considerations concerning the challenge of incorporating social variables into epidemiological models of infectious disease transmission. Glob Public Health 10: 438448.[Crossref] [Google Scholar]
  63. Barnett T, Seeley J, Levin J, Katongole J, , 2015. Hope: a new approach to understanding structural factors in HIV acquisition. Glob Public Health 10: 417437.[Crossref] [Google Scholar]
  64. Biran A, Schmidt WP, Varadharajan KS, Rajaraman D, Kumar R, Greenland K, Gopalan B, Aunger R, Curtis V, , 2014. Effect of a behaviour-change intervention on handwashing with soap in India (SuperAmma): a cluster-randomised trial. Lancet Glob Health 2: e145e154.[Crossref] [Google Scholar]
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  • Received : 08 Jan 2017
  • Accepted : 24 Mar 2017

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