title: Intervention strategies to reduce the risk of zoonotic infection with avian influenza viruses: scientific basis, challenges and knowledge gaps.
abstract: A range of measures has been recommended and used for the control and prevention of avian influenza. These measures are based on the assessment of local epidemiological situations, field observations and other scientific information. Other non-technical factors are (or in some cases should be) taken into account when developing and recommending control measures. The precise effects under field conditions of most individual interventions applied to control and prevent avian influenza have not been established or subjected to critical review, often because a number of measures are applied simultaneously without controls. In most cases, the combination of measures used results in control or elimination of the virus although there are some countries where this has not been the case. In others, especially those with low poultry density, it is not clear whether the link between the adoption of a set of measures and the subsequent control of the disease is causative. This article discusses the various measures recommended, with particular emphasis on stamping out and vaccination, examines how these measures assist in preventing zoonotic infections with avian influenza viruses and explores gaps in knowledge regarding their effectiveness.
authors.affiliation: Asia Pacific Veterinary Information Services, Montmorency, Vic., Australia.
authors.forename: Leslie D
authors.initials: LD
authors.lastname: Sims
mesh_terms: D000818:Animals; D001717:Birds; D003140:Communicable Disease Control / Q000379:methods*; D006801:Humans; D005585:Influenza in Birds / Q000635:transmission*; D007251:Influenza, Human / Q000517:prevention & control*; D015047:Zoonoses / Q000517:prevention & control*
keywords: Avian influenza; H5N1; control; highly pathogenic avian influenza; prevention; zoonotic
references.citation: Van Kerkhove MD, Mumford E, Mounts AW et al. Highly pathogenic avian influenza (H5N1): pathways of exposure at the animal-human interface, a systematic review. PLoS ONE 2011; 6:e14582.
references.citation: Sims L. Strategies for controlling animal influenza and implications for human health. Influenza Other Respi Viruses 2010; 5(Suppl 1):2-53.
references.citation: Shortridge KF. Poultry and the influenza H5N1 outbreak in Hong Kong, 1997: abridged chronology and virus isolation. Vaccine 1999; 17(Suppl 1):S26-S29.
references.citation: Chen H, Deng G, Li Z et al. The evolution of H5N1 influenza viruses in ducks in southern China. Proc Natl Acad Sci USA 2004; 101:10452-10457.
references.citation: Sims LD, Domenech J, Benigno C et al. Origin and evolution of highly pathogenic H5N1 avian influenza in Asia. Vet Rec 2005; 157:159-164.
references.citation: Gilbert M, Chaitaweesub P, Parakamawongsa T et al. Free-grazing ducks and highly pathogenic avian influenza, Thailand. Emerg Infect Dis 2006; 12:227-234.
references.citation: Martin V, Zhou X, Marshall E et al. Risk-based surveillance for avian influenza control along poultry market chains in South China: the value of social network analysis. Prev Vet Med 2011; 102:196-205.
references.citation: Wan XF, Dong L, Lan Y et al. Indications that live poultry markets are a major source of human H5N1 influenza virus infection in China. J Virol 2011; 85:13422-13438.
references.citation: Hogerwerf L, Wallace RG, Ottaviani D et al. Persistence of highly pathogenic avian influenza H5N1 virus defined by agro-ecological niche. EcoHealth 2010; 7:213-225.
references.citation: Paul M, Tavornpanich S, Abrial D et al. Anthropogenic factors and the risk of highly pathogenic avian influenza H5N1: prospects from a spatial-based model. Vet Res 2010; 41:28.
references.citation: Ottaviani D, de la Rocque S, Khomenko S et al. The cold European winter of 2005-2006 assisted the spread and persistence of H5N1 influenza virus in wild birds. EcoHealth 2010; 7:226-236.
references.citation: Sakoda Y, Ito H, Uchida Y et al. Reintroduction of H5N1 highly pathogenic avian influenza virus by migratory water birds, causing poultry outbreaks in the 2010-2011 winter season in Japan. J Gen Virol 2012; 93:541-550.
references.citation: FAO. Recommendations on the prevention, control and eradication of H5N1 highly pathogenic avian influenza in Asia. 2004. Available at http://www.fao.org/docs/eims/upload/246982/aj126e00.pdf (Accessed 5 September 2012).
references.citation: FAO. FAO/OIE Global strategy for prevention and control of H5N1 highly pathogenic avian influenza. 2008. Available at ftp://ftp.fao.org/docrep/fao/011/aj134e/aj134e00.pdf (Accessed 10 September 2012).
references.citation: OIE. Avian influenza portal. 2011. Available at http://www.oie.int/en/animal-health-in-the-world/web-portal-on-avian-influenza/global-strategy/ (Accessed 5 June 2012).
references.citation: Halvorson DA. Prevention and management of avian influenza outbreaks: experiences from the United States of America. Rev Sci Tech 2009; 28:359-369.
references.citation: OIE. World animal health information system. 2011. Available at http://web.oie.int/wahis/public.php?page=home (Accessed 10 February 2012).
references.citation: FAO. A value chain approach to animal diseases risk management. 2011. Available at www.fao.org/docrep/014/i2198e/i2198e00.pdf (Accessed 10 September 2012).
references.citation: Rich KM, Perry BD. The economic and poverty impacts of animal diseases in developing countries: new roles, new demands for economics and epidemiology. Prev Vet Med 2011; 101:133-147.
references.citation: Sims LD. Lessons learned from Asian H5N1 outbreak control. Avian Dis 2007; 51(Suppl 1):174-181.
references.citation: Sproul T, Zilberman D, Ifft J, Roland-Holst D, Otte J. Economics of avian flu policy. 2009. Available at http://www.dfid.gov.uk/r4d/PDF/Outputs/HPAI/FAO_2009_HPAI_rbr18.pdf (Accessed 10 September 2012).
references.citation: Sims LD. Progress in control of H5N1 highly pathogenic avian influenza. Avian Dis 2012; 56:829-835.
references.citation: FAO. Approaches to controlling, preventing and eliminating H5N1 highly pathogenic avian influenza in endemic countries. 2011. Available at http://www.fao.org/docrep/014/i2150e/i2150e.pdf (Accessed 5 September 2012).
references.citation: Pongcharoensuk P, Adisasmito W, Sat LM et al. Avian and pandemic human influenza policy in South-East Asia: the interface between economic and public health imperatives. Health Policy Plan 2011; 27:374-383.
references.citation: Safman RM. Avian influenza control in Thailand: balancing the interests of different poultry producers; in Scoons I (ed.): Avian Influenza: Science, Policy and Politics. London: Earthscan, 2010; 169-206.
references.citation: Sims LD, Ellis TM, Liu KK et al. Avian influenza in Hong Kong 1997-2002. Avian Dis 2003; 47(Suppl 3):832-838.
references.citation: Domenech J, Dauphin G, Rushton J et al. Experiences with vaccination in countries endemically infected with highly pathogenic avian influenza: the Food and Agriculture Organization perspective. Rev Sci Tech 2009; 28:293-305.
references.citation: Knight-Jones TJ, Gibbens J, Wooldridge M, Stark KD. Assessment of farm-level biosecurity measures after an outbreak of avian influenza in the United Kingdom. Transbound Emerg Dis 2011; 58:69-75.
references.citation: Kaleta EF, Kuczka A, Kuhnhold A et al. Outbreak of duck plague (duck herpesvirus enteritis) in numerous species of captive ducks and geese in temporal conjunction with enforced biosecurity (in-house keeping) due to the threat of avian influenza A virus of the subtype Asia H5N1. Dtsch Tierarztl Wochenschr 2007; 114:3-11.
references.citation: Aral Y, Yalcin C, Cevger Y, Sipahi C, Sariozkan S. Financial effects of the highly pathogenic avian influenza outbreaks on the Turkish broiler producers. Poult Sci 2010; 89:1085-1088.
references.citation: Martin V, Pfeiffer DU, Zhou X, Xiao X, Prosser DJ, Guo F, Gilbert M. Spatial distribution and risk factors of highly pathogenic avian influenza (HPAI) H5N1 in China. PLoS Pathog 2011; 7:e1001308.
references.citation: Sultana R, Rimi NA, Azad S et al. Bangladeshi backyard poultry raisers’ perceptions and practices related to zoonotic transmission of avian influenza. J Infect Dev Ctries 2012; 6:156-165.
references.citation: Wiegers E, Curry J. Understanding smallholders’ decisions towards adopting HPAI prevention and control measures. 2009. Available at http://aphca.org/dmdocuments/RBR_16_HPAI%20&%20Livelihoods_Wiegers_090528.pdf (Accessed 15 September 2012).
references.citation: FAO. How can animal health systems support small scale producers and traders? 2012. Available at www.fao.org/docrep/015/i2739e/i2739e00.pdf (Accessed 15 September 2012).
references.citation: Bett B, Okike I, Unger F, Randolph T. Alignment of poultry sector actors with avian influenza control. 2010. Available at http://www.dfid.gov.uk/r4d/PDF/Outputs/HPAI/PRE101025_Bett_Institutions.pdf (Accessed 18 September 2012).
references.citation: Bowes VA. After the outbreak: how the British Columbia commercial poultry industry recovered after H7N3 HPAI. Avian Dis 2007; 51(Suppl 1):313-316.
references.citation: Stegeman A, Bouma A, Elbers AR et al. Avian influenza A virus (H7N7) epidemic in The Netherlands in 2003: course of the epidemic and effectiveness of control measures. J Infect Dis 2004; 190:2088-2095.
references.citation: FAO. Empress Watch. Highly pathogenic avian influenza in Mexico. 2012. Available at http://www.fao.org/docrep/016/an395e/an395e.pdf (Accessed 10 October 2012).
references.citation: Sims LD, Brown IH. Multicontinental epidemic of H5N1 HPAI virus; in Swayne D (ed.): Avian Influenza. Iowa: Blackwell Ames, 2008; 251-286.
references.citation: Stegeman JA, Bouma A, de Jong MC. Epidemiological models to assist the management of highly pathogenic avian influenza. Rev Sci Tech 2011; 30:571-579.
references.citation: Te Beest DE, Hagenaars TJ, Stegeman JA, Koopmans MP, van Born M. Risk based culling for highly infectious diseases of livestock. Vet Res 2011; 42:81.
references.citation: Sharkey KJ, Bowers RG, Morgan KL, Robinson SE, Christley RM. Epidemiological consequences of an incursion of highly pathogenic H5N1 avian influenza into the British poultry flock. Proc Biol Sci 2008; 275:19-28.
references.citation: Truscott J, Garske T, Chis-Ster I et al. Control of a highly pathogenic H5N1 avian influenza outbreak in the GB poultry flock. Proc Biol Sci 2007; 274:2287-2295.
references.citation: Gutiérrez RA, Buchy P. Contaminated soil and transmission of influenza virus (H5N1). Emerg Infect Dis 2012; 18:1530-1532.
references.citation: Kapur VS. Responding to the challenge of bird flu in rural property - insights from West Bengal. 2008. Available at http://www.dfid.gov.uk/r4d/PDF/Outputs/HPAI/WestBengalProducer.pdf (Accessed 10 September 2012).
references.citation: World Bank. Enhancing Control of Highly Pathogenic Avian Influenza in Developing Countries through Compensation: Issues and Good Practices. Washington, DC: World Bank, 2006. Available at http://siteresources.worldbank.org/INTARD/Resources/HPAI_Compensation_Final.pdf (Accessed 5 September 2012).
references.citation: Phan MQ, Henry W, Bui CB et al. Detection of HPAI H5N1 viruses in ducks sampled from live bird markets in Vietnam. Epidemiol Infect 2012; 1:1-11.
references.citation: Van Kerkhove MD, Ly S, Guitian J et al. Changes in poultry handling behavior and poultry mortality reporting among rural Cambodians in areas affected by HPAI/H5N1. PLoS ONE 2009; 4:e6466.
references.citation: Ear S. Cambodia's victim zero: global and national responses to highly pathogenic avian influenza. STEPS centre. 2009. Available at http://steps-centre.org/wpsite/wp-content/uploads/Cambodia-new.pdf ISBN 978 1 85864 581 6 (Accessed 20 September 2012).
references.citation: Bett B, Henning J, Abdu P et al. Transmission rate and reproductive number of the H5N1 highly pathogenic avian influenza virus during the December 2005-July 2008 epidemic in Nigeria. Transbound Emerg Dis 2012 Aug 27. doi: 10.1111/tbed.12003. [Epub ahead of print].
references.citation: Yalcin C, Sipahi C, Aral Y, Cevger Y. Economic effect of the highly pathogenic avian influenza H5N1 outbreaks among turkey producers, 2005-06, Turkey. Avian Dis 2010; 54(Suppl 1):390-393.
references.citation: Hamilton K, Bruckner G. Good governance for early detection and response. Avian Dis 2010; 54(Suppl 1):384-386.
references.citation: European Reference Laboratory for Avian Influenza: Avian influenza surveillance in the European Union during 2010. 2011. Available at http://ec.europa.eu/food/committees/regulatory/scfcah/animal_health/presentations/0405102011_ai_eu_en.pdf (Accessed 7 September 2012).
references.citation: OFFLU. Strategy document for surveillance and monitoring of influenza in animals. 2010. Available at http://www.offlu.net/fileadmin/home/en/publications/pdf/OFFLUsurveillance.pdf (Accessed 5 September 2012).
references.citation: Cameron A. Surveillance needs tools and options: experiences between developed and developing worlds: 2011: 91-94: In: Proceedings of FAO Animal Health and Production Challenges of Animal Disease Information and Systems for Animal Diseases and Zoonoses. 2010 23-26 November, Rome, Italy. Available at http://www.fao.org/docrep/014/i2415e/i2415e00.pdf (Accessed 20 September 2012).
references.citation: Azhar M, Lubis AS, Siregar ES et al. Participatory disease surveillance and response in Indonesia: strengthening veterinary services and empowering communities to prevent and control highly pathogenic avian influenza. Avian Dis 2010; 54:749-753.
references.citation: Daniels P, Wiyono A, Sawitri E, Poermadjaja B, Sims LD. H5N1 highly pathogenic avian influenza in Indonesia: retrospective considerations. Curr Top Microbiol Immunol 2012 Sep 6. [Epub ahead of print]. PMID: 22956392.
references.citation: Capua I, Schmitz A, Jestin V, Koch G, Marangon S. Vaccination as a tool to combat introductions of notifiable avian influenza viruses in Europe, 2000 to 2006. Rev Sci Tech 2009; 28:245-259.
references.citation: Gonzales JL, Elbers AR, Bouma A, Koch G, de Wit JJ, Stegeman JA. Transmission characteristics of low pathogenic avian influenza virus of H7N7 and H5N7 subtypes in layer chickens. Vet Microbiol 2011; 155:207-213.
references.citation: Shi H, Ashraf S, Gao S, Lu J, Liu X. Evaluation of transmission route and replication efficiency of H9N2 avian influenza virus. Avian Dis 2010; 54:22-27.
references.citation: CAST. 2007. Avian Influenza Vaccines: Focusing on H5N1 High Pathogenicity Avian Influenza (HPAI).
references.citation: OIE. Vaccine Bank. 2011. Available at http://www.oie.int/en/support-to-oie-members/vaccine-bank/ (Accessed 10 September 2012).
references.citation: Hamilton SA. Simulating the transmission and control of highly pathogenic avian influenza epidemics in the Australian poultry industries. Ph.D. Thesis, University of Sydney, Australia. 2011.
references.citation: Hinrichs J, Otte J, Rushton J. Technical, epidemiological and financial implications of large-scale national vaccination campaigns to control HPAI H5N1. CAB Reviews 2010; 5:1-21.
references.citation: Chen H. Avian influenza vaccination: the experience in China. Rev Sci Tech 2009; 28:267-274.
references.citation: Peyre M, Samaha H, Makonnen YJ et al. Avian influenza vaccination in Egypt: limitations of the current strategy. J Mol Genet Med 2009; 3:198-204.
references.citation: FAO. Gathering evidence for a transitional strategy (GETS) for HPAI H5N1 vaccination in Viet Nam. 2012. Available at http://www.fao.org/fileadmin/user_upload/faovn/docs/GETS%20Brochure-FAO%20Vietnam_Final.pdf (Accessed 10 September 2012).
references.citation: Abdelwhab EM, Grund C, Aly MM, Beer M, Harder TC, Hafez HM. Influence of maternal immunity on vaccine efficacy and susceptibility of one day old chicks against Egyptian highly pathogenic avian influenza H5N1. Vet Microbiol 2011; 155:13-20.
references.citation: Poetri O, Bouma A, Claassen I et al. A single vaccination of commercial broilers does not reduce transmission of H5N1 highly pathogenic avian influenza. Vet Res 2011; 42:74.
references.citation: Kim JK, Kayali G, Walker D et al. Puzzling inefficiency of H5N1 influenza vaccines in Egyptian poultry. Proc Natl Acad Sci USA 2010; 107:11044-11049.
references.citation: Eggert D, Swayne DE. Single vaccination provides limited protection to ducks and geese against H5N1 high pathogenicity avian influenza virus. Avian Dis 2010; 54:1224-1229.
references.citation: Kumar M, Chu HJ, Rodenberg J, Krauss S, Webster RG. Association of serologic and protective responses of avian influenza vaccines in chickens. Avian Dis 2007; 51:481-483.
references.citation: Ellis TM, Sims LD, Wong HK et al. Use of avian influenza vaccination in Hong Kong. Dev Biol (Basel) 2006; 124:133-143.
references.citation: Sun S, Cui Z, Wang J, Wang Z. Protective efficacy of vaccination against highly pathogenic avian influenza is dramatically suppressed by early infection of chickens with reticuloendotheliosis virus. Avian Pathol 2009; 38:31-34.
references.citation: Van der Goot JA, Van Born M, Koch G, de Jong MC. Variable effect of vaccination against highly pathogenic avian influenza (H7N7) virus on disease and transmission in pheasants and teals. Vaccine 2007; 25:8318-8325.
references.citation: Cagle C, Wasilenko J, Adams SC et al. Differences in pathogenicity, response to vaccination, and innate immune responses in different types of ducks infected with a virulent H5N1 highly pathogenic avian influenza virus from Vietnam. Avian Dis 2012; 56:479-487.
references.citation: Tian G, Zeng X, Li Y, Shi J, Chen H. Protective efficacy of the H5 inactivated vaccine against different highly pathogenic H5N1 avian influenza viruses isolated in China and Vietnam. Avian Dis 2010; 54:287-289.
references.citation: Lee CW, Senne DA, Suarez DL. Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. J Virol 2004; 78:8372-8381.
references.citation: Cattoli G, Fusaro A, Monne I et al. Evidence for differing evolutionary dynamics of A/H5N1 viruses among countries applying or not applying avian influenza vaccination in poultry. Vaccine 2011; 29:9368-9375.
references.citation: WHO. Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. Wkly Epidemiol Rec 2011; 86:469-480.
references.citation: Liu J, Chen P, Jiang Y et al. A duck enteritis virus-vectored bivalent live vaccine provides fast and complete protection against H5N1 avian influenza virus in ducks. J Virol 2011; 85:10989-10998.
references.citation: Rauw F, Palya V, Van Born S et al. Further evidence of antigenic drift and protective efficacy afforded by a recombinant HVT-H5 vaccine against challenge with two antigenically divergent Egyptian clade 2.2.1 HPAI H5N1 strains. Vaccine 2011; 29:2590-2600.
references.citation: Swayne DE, Suarez DL. Current developments in avian influenza vaccines, including safety of vaccinated birds as food. Dev Biol (Basel) 2007; 130:123-133.
references.citation: Sims LD, Dung DH. Vaccination of poultry in Vietnam against H5N1 highly pathogenic avian influenza. 2009. Available at http://www.aitoolkit.org/site/DefaultSite/filesystem/documents/CASE%20STUDY_07-09-09%20final.pdf (Accessed 10 September 2012).
references.citation: Swayne DE, Pavade G, Hamilton K, Vallat B, Miyagishima K. Assessment of national strategies for control of high-pathogenicity avian influenza and low-pathogenicity notifiable avian influenza in poultry, with emphasis on vaccines and vaccination. Rev Sci Tech 2011; 30:839-870.
references.citation: Desvaux S, Grosbois V, Pham TT et al. Evaluation of the vaccination efficacy against H5N1 in domestic poultry in the Red River Delta in Vietnam. Epidemiol Infect 2012; 30:1-13.
references.citation: Walker PG, Cauchemez S, Metras R, Dung DH, Pfeiffer D, Ghani AC. A Bayesian approach to quantifying the effects of mass poultry vaccination upon the spatial and temporal dynamics of H5N1 in Northern Vietnam. PLoS Comput Biol 2010; 6:e1000683.
references.citation: Lyall J, Irvine RM, Sherman A et al. Suppression of avian influenza transmission in genetically modified chickens. Science 2011; 331:223-226.
references.citation: Fasina FO, Ali AM, Yilma JM, Thieme O, Ankers P. The cost-benefit of biosecurity measures on infectious diseases in the Egyptian household poultry. Prev Vet Med 2011; 103:178-191.
references.citation: Abdelwhab EM, Selim AA, Arafa A et al. Circulation of avian influenza H5N1 in live bird markets in Egypt. Avian Dis 2010; 54:911-914.
references.citation: Lau EH, Leung YH, Zhang LJ 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.
references.citation: Leung YH, Lau EHY, Zhang LJ, Guan Y, Cowling BJ, Peiris JSM. Avian influenza and ban on overnight storage in live poultry markets, Hong Kong. Emerg Infect Dis 2012; 18:1339-1341.
references.citation: Sims LD, Peiris M. One health: the Hong Kong experience with avian influenza. Curr Top Microbiol Immunol 2012 Aug 18 [Epub ahead of print]. PMID: 22903569.
references.citation: Sims LD. Risks associated with poultry production systems, in Proceedings Poultry in the 21st Century Avian Influenza and Beyond. 2008. Available at http://www.fao.org/AG/againfo/home/events/bangkok2007/docs/part2/2_1.pdf (Accessed 1 September 2012).
references.citation: Métras R, Stevens KB, Abdu P et al. Identification of potential risk factors associated with highly pathogenic avian influenza subtype H5N1 outbreak occurrence in Lagos and Kano states, Nigeria, during the 2006-2007 epidemics. Transbound Emerg Dis 2013; 60:87-96.
references.citation: Biswas PK, Rahman MH, Das A et al. Risk for highly pathogenic avian influenza H5N1 virus infection in chickens in small-scale commercial farms, in a high-risk area, Bangladesh, 2008. Transbound Emerg Dis 2011; 58:519-525.
references.citation: Desvaux S, Grosbois V, Pham TT et al. Risk factors of highly pathogenic avian influenza H5N1 occurrence at the village and farm levels in the Red River Delta Region in Vietnam. Transbound Emerg Dis 2011; 58:492-502.
references.citation: Paul M, Wongnarkpet S, Gasqui P et al. Risk factors for highly pathogenic avian influenza (HPAI) H5N1 infection in backyard chicken farms, Thailand. Acta Trop 2011; 118:209-216.
references.citation: Fasina FO, Rivas AL, Bisschop SP et al. Identification of risk factors associated with highly pathogenic avian influenza H5N1 virus infection in poultry farms, in Nigeria during the epidemic of 2006-2007. Prev Vet Med 2011; 98:204-208.
references.citation: Mondal SP, Tardif-Douglin D, Ryan-Silva R, Magnani R. Controlling highly pathogenic avian influenza, Bangladesh [letter]. Emerg Infect Dis [Internet]. 2012; 18:2083-2085.
references.citation: Elbers AR, Gorgievski-Duijvesteijn MJ, Zarafshani K, Koch G. To report or not to report: a psychosocial investigation aimed at improving early detection of avian influenza outbreaks. Rev Sci Tech 2010; 29:435-449.
references.citation: FAO. Cleaning and Disinfection of Poultry Farms. 2011. Available at http://www.fao.org/docrep/014/al876e/al87600.pdf (Accessed 10 September 2012).
references.citation: OIE. Infection with viruses of notifiable avian influenza, in Terrestrial Animal Health Code 2012. Available at http://www.oie.int/index.php?id=169&L=0&htmfile=chapitre_1.10.4.htm (Accessed 10 December 2012).