Endemicity of avian influenza in ducks living around commercial layer farms

Simson Tarigan, Risa Indriani, . Sumarningsih


The progenitors of all avian influenza viruses are generally derived from ducks or other waterfowl that have undergone mutation and adaptation to become pathogenic in chickens or other poultry. Investigation of the presence of avian influenza viruses in ducks especially those living around chicken farms is, therefore, important. Serum from 54 ducks and 51 Muscovy ducks living around commercial layer farms in the districts of Cianjur and Sukabumi were collected in March - April 2014. The indication of AI-virus infection in those birds was based on an array of serological tests including competitive and indirect ELISAs for antibody to nucleoprotein, MM2e ELISA for antibody to M2e, HI test, ELISAs and dot blot for antibodies to haemagglutinin, and dot blot assay for antibodies to neuraminidase. Recombinant Haemagglutinins (H1-H13 and H15), recombinant neuraminidases (N1, N2, N7 and N9) and recombinant influenza-A nucleoprotein were used in the indirect ELISAs and dot blot assays. As many as 63% of duck samples and 13% Muscovy-duck samples were serologically positive to nucleoprotein, and 62% of the nucleoprotein-seropositive ducks were also positive to M2e. The high seroprevalence of AI in the ducks living around commercial poultry farms suggested that application of strict biosecurity measures on those farms is still needed. Based on the results of the ELISA and dot blot assays, AI virus subtypes H9N2 and H5N2, in addition to H5N1, were suspected to be circulating in those ducks. Further confirmation by virus isolation, however, is required because H9N2 and H5N2 subtypes have yet been unknown Indonesia and both the subtypes can cause serious disease in poultry.

Key Words: Duck, Immunoassay, Avian Influenza, H5N1, H5N2, H9N2


Duck; Immunoassay; Avian Influenza; H5N1; H5N2; H9N2

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Abolnik C, Olivier AJ, Grewar J, Gers S, Romito M. 2012. Molecular analysis of the 2011 HPAI H5N2 outbreak in ostriches, South Africa. Avian Dis. 56:865-879.

Alexander DJ. 2000. A review of avian influenza in different bird species. Vet Microbiol. 74:3-13.

Banet-Noach C, Perk S, Simanov L, Grebenyuk N, Rozenblut E, Pokamunski S, Pirak M, Tendler Y, Panshin A. 2007. H9N2 influenza viruses from Israeli poultry: a five-year outbreak. Avian Dis. 51:290-296.

Cagle C, To TL, Nguyen T, Wasilenko J, Adams SC, Cardona CJ, Spackman E, Suarez DL, Pantin-Jackwood MJ. 2011. Pekin and Muscovy ducks respond differently to vaccination with a H5N1 highly pathogenic avian influenza (HPAI) commercial inactivated vaccine. Vaccine. 29:6549-6557.

Cameron KR, Gregory V, Banks J, Brown IH, Alexander DJ, Hay AJ, Lin YP. 2000. H9N2 subtype influenza A viruses in poultry in pakistan are closely related to the H9N2 viruses responsible for human infection in Hong Kong. Virology. 278:36-41.

Clement T, Kutish GF, Nezworski J, Scaria J, Nelson E, Christopher-Hennings J, Diel DG. 2015. Complete Genome Sequence of a Highly Pathogenic Avian Influenza Virus (H5N2) Associated with an Outbreak in Commercial Chickens, Iowa, USA, 2015. Genome Announc 3.

DGLAHS. 2013. Livestock and animal health statistics 2013. Jakarta (Indones): Direktorat Jenderal Peternakan dan Kesehatan Hewan, Kementerian Pertanian.

Dharmayanti NLPI, Hartawan R, Pudjiatmoko, Wibawa H, Hardiman, Balish A, Donis R, Davis CT, Samaan G. 2014. Genetic characterization of clade avian influenza A(H5N1) viruses, Indonesia, 2012. Emerg Infect Dis. 20:671-674.

[Ditjennak] Direktorat Jenderal Peternakan. 2013. Perkembangan kasus Avian Influenza (AI) pada unggas kondisi s/d 31 Desember 2013. http://ditjennak.pertanian.go.id, download August 12, 2015.

Ghaniei A, Allymehr M, Moradschendi A. 2013. Seroprevalence of avian influenza (H9N2) in broiler chickens in Northwest of Iran. Asian Pac J Trop Biomed. 3: 822-824.

Guan Y, Smith GJ. 2013. The emergence and diversification of panzootic H5N1 influenza viruses. Virus Res. 178:35-43.

Guo YJ, Krauss S, Senne DA, Mo IP, Lo KS, Xiong XP, Norwood M, Shortridge KF, Webster RG, Guan Y. 2000. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology. 267:279-288.

Hemmatzadeh F, Sumarningsih S, Tarigan S, Indriani R, Dharmayanti NLPI, Ebrahimie E, Igniatovic J. 2013. Recombinant M2e protein-based ELISA: a novel and inexpensive approach for differentiating avian influenza infected chickens from vaccinated ones. PLoS One. 8:e56801.

Henning J, Wibawa H, Morton J, Usman TB, Junaidi A, Meers J. 2010. Scavenging ducks and transmission of highly pathogenic avian influenza, Java, Indonesia. Emerg Infect Dis. 16:1244-1250.

Hotta K, Takakuwa H, Le QM, Phuong SL, Murase T, Ono E, Ito T, Otsuki K, Yamashiro T. 2012. Isolation and characterization of H6N1 and H9N2 avian influenza viruses from Ducks in Hanoi, Vietnam. Virus Res. 163:448-453.

Huddleston JA, Brownlee GG. 1982. The sequence of the nucleoprotein gene of human influenza A virus, strain A.NT/60/68. Nucleic Acid Res. 10:1029-1038.

Jakhesara SJ, Bhatt VD, Patel NV, Prajapati KS, Joshi CG. 2014. Isolation and characterization of H9N2 influenza virus isolates from poultry respiratory disease outbreak. Springerplus. 3:196.

Khatun A, Giasuddin M, Islam KM, Khanom S, Samad MA, Islam MR, Noor M, Bhuiyan JU, Kim WI, Eo SK, Rahman MM. 2013. Surveillance of avian influenza virus type A in semi-scavenging ducks in Bangladesh. BMC Vet Res. 9:196.

Kim JA, Cho SH, Kim HS, Seo SH. 2006. H9N2 influenza viruses isolated from poultry in Korean live bird markets continuously evolve and cause the severe clinical signs in layers. Vet Microbiol. 118:169-176.

Kim,MC, Choi JG, Kwon JS, Kang HM, Paek MR, Jeong OM, Kwon JH, Lee YJ. 2010. Field application of the H9M2e enzyme-linked immunosorbent assay for differentiation of H9N2 avian influenza virus-infected chickens from vaccinated chickens. Clin Vaccine Immunol. 17:1977-1984.

Lambrecht B, Steensels M, Van Borm S, Meulemans G, van den Berg T. 2007. Development of an M2e-specific enzyme-linked immunosorbent assay for differentiating infected from vaccinated animals. Avian Dis. 51:221-226.

Lee CW, Swayne DE, Linares JA, Senne DA, Suarez DL. 2005. H5N2 avian influenza outbreak in Texas in 2004: the first highly pathogenic strain in the United States in 20 years?. J Virol. 79:11412-11421.

Lee YN, Lee DH, Park JK, Lim TH, Youn HN, Yuk SS, Lee YJ, Mo IP, Sung HW, Lee JB, Park SY, ChoI IS, Song CS. 2011. Isolation and characterization of a novel H9N2 influenza virus in Korean native chicken farm. Avian Dis. 55:724-727.

Lin, Shaw YPM, Gregory V, Cameron K, Lim W, Klimov A, Subbarao K, Guan Y, Krauss S, Shortridge K, Webster R, Cox N, Hay A. 2000. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci USA.97:9654-9658.

Loth L, Gilbert M, Wu J, Czarnecki C, Hidayat M, Xiao X. 2011. Identifying risk factors of highly pathogenic avian influenza (H5N1 subtype) in Indonesia. Prev Vet Med. 102:50-58.

Martin V, Sims L, Lubroth J, Pfeiffer D, Slingenbergh J, Domenech J. 2006. Epidemiology and ecology of highly pathogenic avian influenza with particular emphasis on South East Asia. Dev Biol. 124:23-36.

Matrosovich MN, Krauss S, Webster RG. 2001. H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology. 281:156-162.

Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. 1999. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med. 5:1157-1163.

Nguyen T, Davis CT, Stembridge W, Shu B, Balish A, Inui K, Do HT, Ngo HT, Wan XF, McCarron M, Lindstrom SE, Cox NJ, Nguyen CV, Klimov AI, Donis RO. 2009. Characterization of a highly pathogenic avian influenza H5N1 virus sublineage in poultry seized at ports of entry into Vietnam. Virology. 387:250-256.

Nomura N, Sakoda, Endo M, Yoshida H, Yamamoto N, Okamatsu M, Sakurai K, Hoang NV, Nguyen LV, Chu HD, Tien TN, Kida H. 2012. Characterization of avian influenza viruses isolated from domestic ducks in Vietnam in 2009 and 2010. Arch Virol. 157:247-257.

[OCVO] Office of the Chief Veterinary Officer. 2010. National Avian Influenza Surveillance Dossier. Canberra (Australia): Office of the Chief Veterinary Officer, Australian Government Department of Agriculture, Fisheries and Forestry.

[OIE] Office International des Epizooties. 2012. Manual of diagnostic tests and vaccines for terrestrial animals. 7th ed. Office International des Epizooties.

Okamatsu M, Saito T, Yamamoto Y, Mase M, Tsuduku S, Nakamura K, Tsukamoto K, Yamaguchi S. 2007. Low pathogenicity H5N2 avian influenza outbreak in Japan during the 2005-2006. Vet Microbiol. 124:35-46.

Ronohardjo P. 1982. Virus influenza A itik di Indonesia serta pengaruhnya pada kesehatan masyarakat dan ekonomi peternakan (Thesis). Bogor (Indones): Institut Pertanian Bogor.

Sergeant ES, Kirkland PD, Cowled BD. 2009. Field evaluation of an equine influenza ELISA used in New South Wales during the 2007 Australian outbreak response. Prev Vet Med. 92:382-385.

Sergeev AA, Demina OK, Pyankov OV, Pyankova OG, Agafonov AP, Kiselev SA, Agranovski IE, Sergeev AA, Shikov AN, Shishkina LN, Safatov AS, Sergeev AN. 2013. Infection of chickens caused by avian influenza virus A/H5N1 delivered by aerosol and other routes. Transbound Emerg Dis. 60:159-165.

Shehata AA, Parvin R, Sultan H, Halami MY, Talaat S, Abd-Elrazek A, Ibrahim M, Heenemann K, Vahlenkamp T. 2015. Isolation and full genome characterization of avian influenza subtype H9N2 from poultry respiratory disease outbreak in Egypt. Virus Genes. 50:389-400.

Susanti R, Soejono RD, Mahardika GN, Wibawan I-WT. 2008. Prevalence of Avian Influenza Virus Subtype H5n1 in Waterfowl in West Java Province of Indonesia. 13th International Congress on Infectious Diseases, Kuala Lumpur June 19-22, 2008: e127.

Swayne DE. 2007. Understanding the complex pathobiology of high pathogenicity avian influenza viruses in birds. Avian Dis. 51:242-249.

Tarigan S, Indriani R, Durr PA, Ignjatovic J. 2015a. Characterization of the M2e antibody response following highly pathogenic H5N1 avian influenza virus infection and reliability of M2e ELISA for identifying infected among vaccinated chickens. Avian Pathol. 44:259-268.

Tarigan S, Indriani R, Igniatovic J. 2015b. Circulating H5N1 virus among native chicken living around commercial layer farms. JITV. 20:224-232.

Tiensin T, et al. 2007. Geographic and temporal distribution of highly pathogenic avian influenza A virus (H5N1) in Thailand, 2004-2005: an overview. Avian Dis. 51:182-188.

Villareal CL, Flores AO. 1997. The Mexican avian influenza (H5N2) outbreak. Proc. 4th Int. Symp.Avian Influenza, Athen, Georgia, USA May 28-31, 1997:18-22.

Wan XF. 2012. Lessons from emergence of A/goose/Guangdong/1996-like H5N1 highly pathogenic avian influenza viruses and recent influenza surveillance efforts in southern China. Zoonoses Public Health. 59:32-42.

Wang Q, Ju L, Liu P, Zhou J, Lv X, Li L, Shen H, Su H, Jiang L, Jiang Q. 2014. Serological and Virological Surveillance of Avian Influenza A Virus H9N2 Subtype in Humans and Poultry in Shanghai, China, Between 2008 and 2010. Zoonoses Public Health.

Wibawa H, Bingham J, Nuradji H, Lowther S, Payne J, Harper J, Junaidi A, Middleton D, Meers J. 2014. Experimentally infected domestic ducks show efficient transmission of Indonesian H5N1 highly pathogenic avian influenza virus, but lack persistent viral shedding. PLoS One. 9:e83417.

Wibawa H, Bingham J, Nuradji H, Lowther S, Payne J, Harper J, Wong F, Lunt R, Junaidi A, Middleton D, Meers J. 2013. The pathobiology of two Indonesian H5N1 avian influenza viruses representing different clade 2.1 sublineages in chickens and ducks. Comp Immunol Microbiol Infect Dis. 36:175-191.

Woo JT, Park BK. 2008. Seroprevalence of low pathogenic avian influenza (H9N2) and associated risk factors in the Gyeonggi-do of Korea during 2005-2006. J Vet Sci. 9:161-168.

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:e800-805.

Zhu G, Wang R, Xuan F, Daszak P, Anthony SJ, Zhang S, Zhang L, He G. 2013. Characterization of recombinant H9N2 influenza viruses isolated from wild ducks in China. Vet Microbiol. 166:327-336.


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