Open Access
Review (Published online: 08-10-2017)
7. Public health concerns of highly pathogenic avian influenza H5N1 endemicity in Africa
Olubunmi Gabriel Fasanmi, Ismail Ayoade Odetokun, Fatima Adeola Balogun and Folorunso Oludayo Fasina
Veterinary World, 10(10): 1194-1204

Olubunmi Gabriel Fasanmi: Department of Production Animal Studies, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, South Africa; Department of Animal Health, Federal Colleges of Animal Health and Production Technology, Ibadan, Nigeria.
Ismail Ayoade Odetokun: Department of Veterinary Public Health & Preventive Medicine, University of Ilorin, Ilorin, Nigeria.
Fatima Adeola Balogun: Department of Animal Health, Federal Colleges of Animal Health and Production Technology, Ibadan, Nigeria.
Folorunso Oludayo Fasina: Emergency Centre for Transboundary Animal Diseases - Food and Agriculture Organisation, Gigiri, Nairobi, Kenya; Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, South Africa.

doi: 10.14202/vetworld.2017.1194-1204

Share this article on [Facebook] [LinkedIn]

Article history: Received: 24-07-2017, Accepted: 13-09-2017, Published online: 08-10-2017

Corresponding author: Olubunmi Gabriel Fasanmi

E-mail: bumaetal@gmail.com

Citation: Fasanmi OG, Odetokun IA, Balogun FA, Fasina FO (2017) Public health concerns of highly pathogenic avian influenza H5N1 endemicity in Africa, Veterinary World, 10(10): 1194-1204.
Abstract

Highly pathogenic avian influenza virus (HPAIV) H5N1 was first officially reported in Africa in 2006; thereafter this virus has spread rapidly from Nigeria to 11 other African countries. This study was aimed at utilizing data from confirmed laboratory reports to carry out a qualitative evaluation of the factors responsible for HPAI H5N1 persistence in Africa and the public health implications; and to suggest appropriate control measures. Relevant publications were sought from data banks and repositories of FAO, OIE, WHO, and Google scholars. Substantiated data on HPAI H5N1 outbreaks in poultry in Africa and in humans across the world were mined. HPAI H5N1 affects poultry and human populations, with Egypt having highest human cases (346) globally. Nigeria had a reinfection from 2014 to 2015, with outbreaks in Cote d'Ivoire, Ghana, Niger, Nigeria, and Burkina Faso throughout 2016 unabated. The persistence of this virus in Africa is attributed to the survivability of HPAIV, ability to evolve other subtypes through genetic reassortment, poor biosecurity compliance at the live bird markets and poultry farms, husbandry methods and multispecies livestock farming, poultry vaccinations, and continuous shedding of HPAIV, transboundary transmission of HPAIV through poultry trades; and transcontinental migratory birds. There is, therefore, the need for African nations to realistically reassess their status, through regular surveillance and be transparent with HPAI H5N1 outbreak data. Also, it is important to have an understanding of HPAIV migration dynamics which will be helpful in epidemiological modeling, disease prevention, control and eradication measures.

Keywords: Africa, highly pathogenic avian influenza H5N1, public health implications.

References

1. Lekcharoensuk, P. (2008) Highly pathogenic avian influenza (HPAI) H5N1 virus in Asia: Evolution and vaccination. Vet. World, 1(12): 368-374.

2. Kabir, S.M.L. (2010) Avian flu (H5N1): Threat of 'global pandemic' is growing and it's impact on the developing countries' economy. Afr. J. Microbiol. Res., 4(12): 1192-1194.

3. Wahlgren, J. (2011) Influenza a viruses: An ecology review. Inf. Eco. Epidemiol., 1: 6004. [Crossref] [PubMed] [PMC]

4. WHO, World Health Organization. (2014) Avian Influenza Facts Sheets. Available from: http://www.who.int/mediacentre/factsheets/avian_influenza/en. Last accessed on 24-02-2017.

5. OIE, World Organisation for Animal Health. (2014) Highly Pathogenic Avian Influenza, Technical Disease Card. Available from: http://www.oie.int. Last accessed on 24-02-2017.

6. Fasanmi, O.G., Laleye, A.T. and Fasina, F.O. (2016) Systematic review and meta-analyses of cases and deaths associated with HPAI H5N1 in humans and poultry. CAB Rev. Perspect. Agric. Vet. Sci. Nutr. Nat. Resour., 11: 4. [Crossref]

7. Peiris, J.S.M., de Jong, M.D. and Guan, Y. (2007) Avian influenza virus (H5N1): A threat to human health. Clin. Microbiol. Rev., 20(2): 243-267. [Crossref] [PubMed] [PMC]

8. Li, X., Zhang, Z., Yu, A., Ho, S.Y.W., Carr, M.J., Zheng, W., Zhang, Y., Zhu, C., Lei, F. and Shi, W. (2014) Global and local persistence of influenza A(H5N1) virus. Emerg. Infect. Dis., 20(8): 1287-1295. [Crossref] [PubMed] [PMC]

9. USDA, United States Department of Agriculture. (2015) Highly Pathogenic Avian Influenza Standard Operating Procedures: Foreign Animal Disease, Preparedness and Response Plan. p1-21. Available from: https://www.aphis.usda.gov/animal_health/emergency_management/downloads/sop/sop_hpai_e-e.pdf. Last accessed on 15-03-2017.

10. Joannis, T., Lombin, L.H., De Benedictis, P., Cattoli, G. and Capua, I. (2006) Confirmation of H5N1 avian influenza in Africa. Vet. Rec., 158(9): 309-310. [Crossref]

11. Cattoli, G., Monne, I., Fusaro, A., Joannis, T.M., Lombin, L.H., Aly, M.M., Domenech, J.M. and Capua, I. (2009) Highly pathogenic avian influenza virus subtype H5N1 in Africa: A comprehensive phylogenetic analysis and molecular characterization of isolates. PLoS One, 4(3): e4842. Available from: http://www.journals.plos.org/plosone/article?id=10.1371/journal.pone.0004842. Last accessed on 03-03-2017. [Crossref]

12. WHO, World Health Organization. (2015) Cumulative Number of Confirmed Human Cases for Avian Influenza A(H5N1) Reported to WHO, 2003-2015. Available from: http://www.who.int/influenza/human_animal_interface/EN_GIP_20151015cumulativeNumbe rH5N1cases.pdf?ua=1. Last accessed on 15-02-2017.

13. Food and Agriculture Organization of the United Nations. Worries Rise Over Outbreaks of Avian Flu in West Africa. News Article. Available from: http://www.fao.org/news/story/it/item/297715/icode. Last accessed on 15-02-2017.

14. Sims, L.D., Domenech, J., Benigno, C., Kahn, S., Kamata, A., Lubroth, J., Martin, V. and Roeder, P. (2005) Origin and evolution of highly pathogenic H5N1 avian influenza in Asia. Vet. Rec., 157(6): 159-164. [Crossref]

15. Alexander, D.J. and Brown, I.H. (2009) History of highly pathogenic avian influenza. Rev. Sci. Tech. Int. Off. Epizoot., 28: 19-38. [Crossref] [PubMed]

16. Peiris, J.S.M., Guan, Y., Markwell, D., Ghose, P., Webster, R.G. and Shortridge, K.F. (2001) Co-circulation of Avian H9N2 and contemporary "human" H3N2 influenza a viruses in pigs in southeastern China: Potential for genetic reassortment? J. Virol., 75(20): 9679-9686. [Crossref] [PubMed] [PMC]

17. Gilbert, M., Chaitaweesub, P., Parakamawongsa, T., Premashthira, S., Tiensin, T., Kalpravidh, W., Wagner, H. and Slingenbergh, J. (2006) Free-grazing ducks and highly pathogenic avian influenza, Thailand. Emerg. Infect. Dis., 12(2): 227-234. [Crossref] [PubMed] [PMC]

18. Gauthier-Clerc, M., Lebarbenchon, C. and Thomas, F. (2007) Recent expansion of highly pathogenic avian influenza H5N1: A critical review. Proc. Natl. Acad. Sci. United States Am., 149: 202-214. [Crossref]

19. Pfeiffer, D.U., Otte, M.J., Roland-Holst, D., Inui, K., Tung, N. and Ziberman, D. (2011) Implications of global and regional patterns of highly pathogenic avian influenza virus H5N1 clades for risk management. Vet. J., 190: 309-316. Available from: https://www.pdfs.semanticscholar.org/1b55/6782e4201696ac12b6d0b974927c7b1b35ee.pdf. Last accessed on 15-02-2017. [Crossref]

20. Kuchipudi, S.V., Tellabati, M., Sebastian, S., Londt, B.Z., Jansen, C., Vervelde, L., Brookes, S.M. and Brown, I.H. (2014) Highly pathogenic avian influenza virus infection in chickens but not ducks is associated with elevated host immune and pro-inflammatory responses. Vet. Res., 45: 118. Available from: https://www.veterinaryresearch.biomedcentral.com/articles/10.1186/s13567-014-0118-3. Last accessed on 16-02-2017. [Crossref]

21. Fasanmi, O.G., Ahmed, S.S.U., Oladele-Bukola, M.O., El-Tahawy, A.S., Elbestawy, A.R. and Fasina, F.O. (2016) An evaluation of biosecurity compliance levels and assessment of associated risk factors for highly pathogenic avian influenza H5N1 infection of live-bird-markets, Nigeria and Egypt. Acta. Trop., 164: 321-328. [Crossref]

22. Rushton, J., Viscarra, R., Guerne-Bleich, E. and McLeod, A. (2005) Impact of avian influenza outbreaks in the poultry sectors of five south East Asian countries (Cambodia, Indonesia, Lao PDR, Thailand and Vietnam): Outbreak costs, responses and potential long-term control. Worlds Poult. Sci. J., 61: 491-514. [Crossref]

23. Nicita, A. (2007) Avian influenza and poultry trade. Policy Research Working Paper 4551. Development Research Group, The World Bank, Washington, DC. p23.

24. Otte, J., Hinrichs, J., Rushton, J., Roland-Holst, D. and Zilberman, D. (2008 )Impacts of avian influenza virus on animal production in developing countries. CAB Rev. PAVSNNR, 3: 1-18. Available from: http://www.fao.org/docs/eims/upload/251044/aj201e00.pdf. Last accessed on 16-02-2017.

25. Fasina, F.O., Sirdar, M.M. and Bisschop, S.P.R. (2008) The financial cost implications of the highly pathogenic notifiable avian influenza H5N1 in Nigeria. Onderstepoort J. Vet. Res., 75(1): 39-46. [Crossref]

26. FAO, Food and Agriculture Organization of the United Nations. (2015) H5N1 HPAI spread in Nigeria and increased risk for neighbouring countries in West Africa. EMPRES Watch, 32. Available from: http://www.fao.org/documents/card/en/c/332c88fd-b229-4db7-9a0d-0bd92dfd3374. Last accessed on 15-02-2017.

27. OIE, World Organisation for Animal Health. (2015) Update on Highly Pathogenic Avian Influenza in Animals (Type H5 and H7). Available from: http://www.oie.int/animal-health-in-theworld/update-on-avian-influenza/2015. Last accessed on 15-02-2017.

28. FAO, Food and Agriculture Organization of the United Nations. (2015) Global Animal Disease Intelligence Report. Rome, Italy. p2. Available from: http://www.fao.org/3/a-i5119e.pdf. Last accessed on 16-02-2017.

29. Kayali, G., Webby, R.J., Xiong, X., Sherif, L.S., El-Ghafar, E.A. and Ali, M.A. (2010) Prospective study of avian influenza transmission to humans in Egypt. BMC Publ. Health, 10: 685. Available from: http://www.bmcpublichealth.biomedcentral.com/articles/10.1186/1471-2458-10-685. Last accessed on 15-02-2017. [Crossref]

30. OIE, World Organisation for Animal Health. (2016) Update on Highly Pathogenic Avian Influenza in Animals (Type H5 and H7). Available from: http://www.oie.int/animal-health-in-the-world/update-on-avian-influenza/2016. Last accessed on 16-02-2017.

31. Perkins, L.E.L. and Swayne, D.E. (2001) Pathobiology of a/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven Gallinaceous species. Vet. Pathol., 38: 149-164. Available from: https://www.naldc.nal.usda.gov/download/24777/PDF. Last accessed on 13-03-2017. [Crossref]

32. MacDonald, J.M. (2008) The economic organization of U.S. broiler production. Econ. Inf. Bull., 38. Available from: http://www.ers.usda.gov/Publications/EIB38. Last accessed on 15-02-2017.

33. Ito, T., Goto, H., Yamamoto, E., Tanaka, H., Takeuchi, M., Kuwayama, M., Kawaoka, Y. and Otsuki, K. (2001) Generation of a highly pathogenic avian influenza a virus from an avirulent field isolate by passaging in chickens. J. Virol., 75(9): 4439-4443. [Crossref] [PubMed] [PMC]

34. Webster, R.G. and Govorkova, E.A. (2006) H5N1 influenza-continuing evolution and spread. N. Engl. J. Med., 355: 2174-2177. Available from: http://www.nejm.org/doi/full/10.1056/NEJMp068205#t=article. Last accessed on 13-03-2017. [Crossref]

35. Fasina, F.O., Bisschop, S.P. and Webster, R.G. (2007) Avian influenza H5N1 in Africa: An epidemiological twist. Lancet Inf. Dis., 7: 696-697.

36. Alhaji, N.B. and Odetokun, I.A. (2011) Assessment of biosecurity measures against highly pathogenic avian influenza risks in small-scale commercial farms and free-range poultry flocks in the Northcentral Nigeria. Transbound. Emerg. Dis., 58(2): 157-161. [Crossref] [PubMed]

37. Holmes, E.C. (2010) The comparative genomics of viral emergence. Proc. Natl. Acad. Sci. United States Am., 107(1): 1742-1746. [Crossref] [PubMed] [PMC]

38. Taubenberger, J.K. and Kash, J.C. (2010) Influenza virus evolution, host adaptation and pandemic formation. Cell. Host. Microb., 7(6): 440-451. [Crossref] [PubMed] [PMC]

39. Perdue, M.L. (2008) Molecular determinants of pathogenicity for avian influenza viruses. In: In: Swayne, D.E., editor. Avian Influenza. Ch. 2. Blackwell Publishing Ltd., Oxford, UK. [Crossref]

40. Suarez, D.L. (2008) Influenza a virus. In: Swayne, D.E., editor. Avian Influenza. Blackwell Publishing, Oxford. p3-22. [Crossref]

41. McHardy, A.C. and Adams, B. (2009) The role of genomics in tracking the evolution of influenza a virus. PLoS Pathog., 5(10): e1000566. Available from: http://www.journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1000566. Last accessed on 15-02-2017. [Crossref]

42. CFSPH, Iowa State University and Institute for International Cooperation in Animal Biologics. (2014) High Pathogenicity Avian Influenza. Available from: http://www.cfsph.iastate.edu/Factsheets/pdfs/highly_pathogenic_avian_influenza.pdf. Last accessed on 13-03-2017.

43. Stegemen, A. (2016) France gets to grip with avian influenza. World Poult. Available from: http://www.worldpoultry.net/Health/Articles/2016/2/France-gets-to-grips-with-AI-situation-2748806W. Last accessed on 06-04-2017.

44. Arafa, A., Suarez, D.L., Hassan, M.K. and Aly, MM. (2010) Phylogenetic analysis of hemagglutinin and neuraminidase genes of highly pathogenic avian influenza H5N1 Egyptian strains isolated from 2006 to 2008 indicates heterogeneity with multiple distinct sublineages. Avian Dis., 54(1): 345-349. Available from: http://www.bioone.org/doi/abs/10.1637/8927-051509-ResNote.1. Last accessed on 15-02-2017.

45. Le, T.H. and Nguyen, N.T.B. (2014) Evolutionary dynamics of highly pathogenic avian influenza A/H5N1 HA clades and vaccine implementation in Vietnam. Clin. Exp. Vac. Res., 3(2): 117-127. [Crossref] [PubMed] [PMC]

46. de Vries, E., Guo, H., Dai, M., Rottier, P.J.M., van Kuppeveld, F.J.M. and de Haan, C.A.M. (2015) Rapid emergence of highly pathogenic avian influenza subtypes from a subtype H5N1 haemagglutinin variant. Emerg. Inf. Dis., 21(5): 842-846. [Crossref] [PubMed] [PMC]

47. Fan, S., Zhou, L., Wu, D., Gao, X., Pei, E., Wang, T., Gao, Y. and Xia, X. (2014) A novel highly pathogenic H5N8 avian influenza isolated from from wild duck in China. Influenza Other Respir. Viruses, 8: 646-653. [Crossref] [PubMed] [PMC]

48. Jeong, J., Kang, H.M., Lee, E.K., Sung, B.M., Kwon, Y.K., Kim, H.R., Choi, K.S., Kim, J.Y., Lee, H.J. and Moon, O.K. (2014) Highly pathogenic avian influenza virus (H5N8) in domestic poultry and its relationship with migratory birds in South Korea during 2014. Vet. Microbiol., 173: 249-257. [Crossref]

49. Wu, H., Peng, X., Xu, L., Jin, C., Cheng, L. andLu, X. (2014) Novel reassortant influenza A(H5N8) viruses in domestic ducks, eastern China. Emerg. Infect. Dis., 20: 1315-1318. [Crossref] [PubMed] [PMC]

50. Lee, Y.J., Kang, H.M., Lee, E.K., Song, B.M., Jeong, J. and Kwon, Y.K. (2014) Novel reassortant influenza a(H5N8) viruses, South Korea. Emerg. Infect. Dis., 20: 1087-1089. [Crossref] [PubMed] [PMC]

51. OIE, World Organisation for Animal Health. (2017) Update on Avian Influenza in Animals (Types H5 and H7). Available from: http://www.oie.int/en/animal-health-in-the-world/update-on-avian-influenza/2017. Last accessed on 22-08-2017.

52. Kayali, G., Kandeil, A., El-Shesheny, R., Kayed, A.S., Maatouq, A.M., Cai, Z., McKenzie, P.P. and Webby, R.J. (2016) Avian influenza A(H5N1) virus in Egypt. Emerg. Infect. Dis., 22(3): 379-388. [Crossref] [PubMed] [PMC]

53. Le, M.T., Wertheim, H.F., Nguyen, H.D., Taylor, W., Hoang, P.V., Vuong, C.D., Nguyen, H.L., Nguyen, H.L., Nguyen, H.H., Nguyen, T.Q., Nguyen, T.V., Van, T.D., Ngoc, B.T. and Bui, T.N. (2008) Influenza A H5N1 clade 2.3.4 virus with a different antiviral susceptibility profile replaced clade 1 virus in humans in northern Vietnam. PLoS One, 3: e3339. [Crossref] [PubMed] [PMC]

54. Boltz, D., Douangngeun, B., Phommachanh, P., Sinthasak, S., Mondry, R., Obert, C., Seiler, P., Keating, R., Suzuki, Y., Hiramatsu, H., Govorkova, E.A. and Webster, R.G. (2010) Emergence of H5N1 avian influenza viruses with reduced sensitivity to neuraminidase inhibitors and novel reassortants in Lao people's democratic republic. J. Gen. Virol., 91: 949-959. Available from: http://www.microbiologyresearch.org/docserver/fulltext/jgv/91/4/949.pdf?expires=1486299204&id=id&accname=guest&checksum=865D41A2186DD459DA3A7BA99DA63091. Last accessed on 16-02-2017. [Crossref]

55. FAO, Food and Agriculture Organization of the United Nations. (2008) Global Programme for the Prevention and Control of H5N1 Highly Pathogenic Avian In?uenza. Available from: ftp://www.ftp.fao.org/docrep/fao/010/ai380e/ai380e00.pdf. Last accessed on 16-02-2017.

56. Kung, N.Y., Guan, Y., Perkins, N.R., Bissett, L., Ellis, T., Sims, L., Morris, R.S., Shortridge, K.F. and Peiris, J.S. (2003) The impact of a monthly rest day on avian influenza virus isolation rates in retail live poultry markets in HongKong. Avian Dis., 47(3): 1037-1041. [Crossref] [PubMed]

57. Webster, R.G. (2004) Wet markets-a continuing source of severe acute respiratory syndrome andinfluenza? Lancet, 363(9404): 234-236.

58. Wang, M., Di, B., Zhou, D.H., Zheng, B.J., Jing, H., Lin, Y.P., Wu, X.W., Qin, P.Z., Wang, Y.L. and Jian, L.Y. (2006) Food markets with live birds as source of avian influenza. Emerg. Infect. Dis., 12(11): 1773-1775. [PubMed] [PMC]

59. Indriani, R., Samaan, G., Gultom, A., Loth, L., Irianti, S., Indryani, S. and Adjid, R. (2010) Environmental sampling for avian influenza virus A (H5N1) in live-bird markets, Indonesia. Emerg. Infect. Dis., 16(12): 1889-1895. [Crossref] [PubMed] [PMC]

60. Wan, X., Dong, L., Lan, Y., Long, L., Xu, C., Zou, S., Wen, L., Cai, Z., Wang, W. and Li, X. (2011) Indications that live poultry markets are a major source of human infection in China. J. Virol., 85(24): 13432-13438. [Crossref] [PubMed] [PMC]

61. Pagani, P., Abimiku, Y. and Emeka-Okolie, W. (2008) Assessment of the Nigerian Poultry Market Chain to Improve Biosecurity. FAO, Rome. Available from: http://www.fao.org/3/a-ak778e.pdf. Last accessed on 15-02-2017.

62. Fasina, F.O., Njage, P.M.K., Ali, A.M.M., Yilma, J.M., Bwala, D.G., Rivas, A.L. and Stegeman, A.J. (2015) Development of disease specific, context specific surveilance models: Avian influenza (H5N1)-related risks and behaviours in African countries. ZPH, 63: 20-33.

63. ElMasry, I., El-Sheikh, H., Abdelnabi, A., Saad, A., Arafa, A., Fasina, F.O., Lubroth, J. and Jobre, YM. (2017) Avian influenza H5N1 surveillance and its dynamics in poultry in live bird markets. Egypt. Transbound Emerg. Dis., 64: 805-814. [Crossref] [PubMed]

64. Cardona, C., Yee, K. and Carpenter, T. (2009) Are live bird markets reservoirs for avian influenza? Poult. Sci., 88(4): 856-859. Available from: https://www.academic.oup.com/ps/article/88/4/856/1557625/Are-live-bird-markets-reservoirs-of-avian. Last accessed on 15-02-2017.

65. CDC, Centre for Disease Control and Prevention. (2015) Avian Influenza in Birds. Avian Influenza in Wild Birds CDC 24/7. Available from: http://www.cdc.gov/flu/avianflu/avian-in-birds.htm. Last accessed on 16-02-2017.

66. Rivas, A.L., Chowell, G., Schwager, S., Fasina, F.O., Hoogesteijn, A.L., Smith, S.D, Bisschop, S.P.R. and Anderson, K.L. (2010) Lessons from Nigeria: The role of roads in the geo-temporal progression of avian influenza (H5N1) virus. Epidemiol. Infect., 138: 192-198. [Crossref]

67. Sonaiya, E.B. and Swan, S.E.J. (2004) Small-Scale Poultry Production. FAO, Rome. Available from: http://www.fao.org/3/a-y5169e.pdf. Last accessed on 17-03-2017.

68. Pym, R., Guerne, B.E. and Hoffmann, I. (2006) The relative contribution of indigenous chicken breeds to poultry meat and egg production and consumption in the developing countries of Africa and Asia. In: 12th European Poultry Conference. World's Poult Sci Assoc., Italy. p197.

69. Sonaiya, F. (2007) Smallholder family poultry as a tool to initiate rural development. In: International Conference Poultry in the Twenty-First Century: Avian Influenza and Beyond: 5-7 November. FAO, Bangkok, Thailand.

70. Minga, U., Msoffe, P.L. and Gwakisa, P.S. Biodiversity (variation) in disease resistance and in pathogens within rural chicken population. In: 22nd World's Poultry Congress: June 8-12. World's Poult Sci Assoc., Istanbul, Turkey.

71. Singh, D.P. and Fotsa, J.C. (2011) Opportunities of poultry breeding programmes for family production in developing countries: The bird for the poor. In: E-Conference of the International Network for Family Poultry Development, 24 January, 18 February. p1-18.

72. Gueye, E.F. (2005) Gender aspects in family poultry management systems in developing countries. Worlds Poult. Sci. J., 61: 39-46. [Crossref]

73. Dorea, F.C., Berghaus, R., Hofacre, C. and Cole, D.J. (2010) Surveys of biosecurity protocols and practices adopted by growers on commercial poultry farms in Georgia, USA. Avian Dis., 54(3): 135-139. [Crossref] [PubMed]

74. Julien, D. and Thompson, S. (2011) Interactive methods to educate and engage poultry producers on the importance of practicing on-farm Biosecurity. J. Agric. Ext. Rural Dev., 3: 137-140. Available from: http://www.academicjournals.org/article/article1379696346_Julien%20and%20Thomson.pdf. Last accessed on 15-02-2017.

75. Zavala, L.A. (2011) Viral Respiratory Diseases of Poultry: A Continuous Challenge. Proceedings of the 17th Congress of the World Vet Poult Assoc., Cancun, Mexico.

76. Conan, A., Goutard, F.L., Sorn, S. and Vong, S. (2012) Biosecurity measures for backyard poultry in developing countries: A systematic review. BMC Vet. Res., 8: 240. Available from: http://www.bmcvetres.biomedcentral.com/articles/10.1186/1746-6148-8-240. Last accessed on 15-02-2017. [Crossref]

77. Abdelqader, A., Wollny, C.B. and Gauly, M. (2007) Characterization of local chicken production systems and their potential under different levels of management practice in Jordan. Trop. Anim. Health Prod., 39(3): 155-164. [Crossref]

78. Badubi, S.S., Ravindran, V. and Reid, J. (2004) A survey of small-scale broiler production systems in Botswana. Trop. Anim. Health Prod., 36(8): 823-834. [Crossref]

79. Biswas, P.K., Uddin, G.M., Barua, H., Roy, K., Biswas, D., Ahad, A., Ahed, A. and Debnath, N.C. (2008) Survivability and causes of loss of broody-hen chicks on smallholder households in Bangladesh. Prev. Vet. Med., 83(3-4): 260-271. [Crossref] [PubMed]

80. Bell, J.G. Factors limiting production efficiency and profitability from smallholder poultry production. Worlds Poult. Sci. J., 65: 207-210. Available from: https://www.cambridge.org/core/journals/world-s-poultry-science-journal/article/div-classtitlefactors-limiting-production-efficiency-and-profitability-from-smallholder-poultry-productiondiv/73406D5CCD1F8FDC275143918D71AB52. Last accessed on 15-02-2017.

81. Fasina, F.O., Ali, A.M., Yilma, J.M., Thieme, O. and Ankers, P. (2012) The cost-benefit of biosecurity measures on infectious diseases in the Egyptian household poultry. Prev. Vet. Med., 103: 178-191. [Crossref] [PubMed]

82. Arafa, A., Naguib, M., Luttermann, C., Selim, A., Kilany, W., Hagag, N., Samy, A., Abdelhalim, A., Hassan, M.K., Abdelwhab, E.M. and Makonnen, Y. (2015) Emergence of a novel cluster of influenza A (H5N1) virus clade 2.2. 1.2 with putative human health impact in Egypt. Eurosurveillance, 20: 2-8. [Crossref] [PubMed]

83. Arafa, A., El-Masry, I., Khoulosy, S., Hassan, M.K., Soliman, M., Fasanmi, O.G., Fasina, F.O., Dauphin, G., Lubroth, J. and Jobre, Y.M. (2016) Predominance and geo-mapping of avian influenza H5N1 in poultry sectors in Egypt. Geospat. Health, 11: 492. [Crossref] [PubMed]

84. CIDRAP, Centre for Infectious Disease Research and Policy. (2016) Avian Flu in Germany and France. Available from: http://www.cidrap.umn.edu/news-perspective/2016/12/more-avian-flu-reported-germany-france. Last accessed on 15-03-2017.

85. European Commission, EC. (2016) Avian Influenza: Latest Development. Available from: http://www.ec.europa.eu/food/animals/animal-diseases/control-measures/avian-influenza_en. Last accessed on 15-02-2017.

86. Capua, I. and Alexander, D.J. (2009) Avian influenza infection in birds: A challenge and opportunity for the poultry veterinarian. Poult. Sci., 88(4): 842-846. [Crossref] [PubMed]

87. Ellis, T.M., Leung, C., Chow, M.K.W., Bissett, L.A., Wong, W., Guan, Y. and Peiris, J.S.M. (2004) Vaccination of chickens against H5N1 avian influenza in the face of an outbreak interrupts virus transmission. Avian Pathol., 33: 405-412. Available from: http://www.tandfonline.com/doi/full/10.1080/03079450410001724012. Last accessed on 14-04-2017. [Crossref]

88. Toro, H. and Tang, D.C. (2009) Protection of chickens against avian influenza with nonreplicating adenovirus-vectored vaccine1. Poult. Sci., 88(4): 867-871. Available from: https://www.academic.oup.com/ps/article/88/4/867/1557642/Protection-of-chickens-against-avian-influenza. Last accessed on 15-02-2017.

89. Peyre, M., Samaha, H., Makonnen, Y.J., Saad, A., Abd-Elnabi, A., Galal, S., Ettel, T., Dauphin, G., Lubroth, J., Roger, F. and Domenech, J. (2009) Avian influenza vaccination in Egypt: Limitations of the current strategy. J. Mol. Genet. Med., 3(2): 198-204. [PubMed] [PMC]

90. Hilleman, M.R. (2002) Realities and enigmas of human viral influenza: Pathogenesis, epidemiology and control. Vaccine, 20(25-26): 3068-3087. [Crossref]

91. Yakubu, B., Nok, A.J., Owolodun, O.A., Luka, P.D. and Umaru, D.A. (2015) The re-occurrence of H5N1 outbreaks necessitates the development of safe and effective influenza vaccine technologies for the prevention and control of avian influenza in Sub-Saharan Africa. Biotech. Mol. Biol. Rev., 10(3): 19-36. Available from: http://www.academicjournals.org/journal/BMBR/article-abstract/9AA790354184. Last accessed on 15-02-2017.

92. ECDC, European Centre for Disease Prevention and Control. (2015) Human Infection with Avian Influenza A (H5N1) Virus, Egypt-First. ECDC, Stockholm. Available from: http://www.ecdc.europa.eu/en/publications/Publications/Rapid-Risk-Assessment-Influenza-A-H5N1-Egypt-March-2015.pdf. Accessed on 13-03-2015.

93. Kilany, W.H., Safwat, M., Mohammed, S.M., Salim, A., Fasina, F.O., Fasanmi, O.G. and Shalaby, A.G. (2016) Protective efficacy of recombinant turkey herpes virus (rHVT-H5) and inactivated H5N1 vaccines in commercial mulard ducks against the highly pathogenic avian influenza (HPAI) H5N1 clade 2.2.1 virus. PLoS One, 11(6): e0156747. [Crossref]

94. FAO, Food and Agriculture Organization of the United Nations. (2011) Approaches to Controlling, Preventing and Eliminating H5N1 Highly Pathogenic Avian Influenza in Endemic Countries. FAO, Rome, Italy. Available from: http://www.fao.org/docrep/014/i2150e/i2150e00.htm. Last accessed on 15-02-2017.

95. Zhang, H., Wang, L., Compans, R.W. and Wang, B.Z. (2014) Universal influenza vaccines, a dream to be realized soon. Viruses, 6(5): 1974-1991. [Crossref] [PubMed] [PMC]

96. Joost, D.P. (2008) Avian Influenza in Zoo and Wild Animal Medicine. 6th ed. Available from: http://www.sciencedirect.com/topics/immunology-and-microbiology/heterologous-vaccine. Last accessed on 14-04-2017.

97. Savill, N.J., Rose, S.G., Keeling, M.J. and Woolhouse, M.E. (2006), Silent spread ofH5N1in vaccinated poultry. Nature, 442(7104): 757-757. [Crossref] [PubMed]

98. Iwami, S., Suzuki, T. and Takeuchi, Y. Paradox of vaccination: Is vaccination really effective against avian flu epidemics? PLoS One, 4: e4915. Available from: http://www.journals.plos.org/plosone/article?id=10.1371/journal.pone.0004915. Last accessed on 15-02-2017.

99. Webster, R., Peiris, M., Chen, H. and Guan, Y. (2006) H5N1 outbreaks and enzootic influenza. Emerg. Infect. Dis., 12(1): 3-8. [Crossref] [PubMed] [PMC]

100. Chen, H., Smith, G., Li, K., Fan, S.H., Rayner, J.M., Vijaykrishna, D., Cheung, C.L. and Huang, K. (2006) Establishment of multiple sublineages of H5N1 influenza virus in Asia: Implications for pandemic control. Proc. Natl. Acad. Sci., 103: 2845-2850. [Crossref] [PubMed] [PMC]

101. Swayne, D.E. (2015) Epidemiology of avian influenza in agricultural and other man-made systems. Avian Influenza. Blackwell Publishing, Ames, IA. p59-85.

102. Ungchusak, K.P., Auewarakul, S.F., Dowell, R., Kitphati, W., Auwanit, P., Puthavathana, M., Uiprasertkul, M., Boonnak, K., Pittayawonganon, C. and Cox, N.J. (2005) Probable person-to-person transmission of avian influenza A (H5N1). N. Engl. J. Med., 352(4): 333-340. [Crossref] [PubMed]

103. Kaplan, B.S. and Webby, R.J. (2013) The avian and mammalian host range of highly pathogenic avian H5N1 influenza. Virus Res., 178(1): 3-11. [Crossref] [PubMed] [PMC]

104. United Nations (UN) Food and Agriculture Organization (FAO). (2015) Questions and Answers: The Facts of Bird Flu. Available from: http://www.fao.org/avianflu/en/qanda.html. Last accessed on 14-04-2017.

105. Stevens, K.B., Costard, S., Metras, R. and Pfeiffer, D.U. (2009) Controlling Avian Flu and Protecting People's Livelihoods in Africa and Indonesia, Using Multicriteria Decision Modelling, HPAI Research Brief No. 7.

106. Martin, V., Pfeiffer, D.U., Zhou, X., Xiao, X., Prosser, D.J., Guo, F., Epprecht, M. and Boles, S. (2011) Spatial distribution and risk factors of highly pathogenic avian influenza (HPAI) H5N1 in China. PLoS Pathog., 7(3): e1001308. Available from: http://www.journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1001308. Last accessed on 15-02-2017. [Crossref]