doi: 10.14202/vetworld.2017.695-701
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Article history: Received: 05-01-2017, Accepted: 05-05-2017, Published online: 25-06-2017
Corresponding author: Hanaa Mohamed Fadel
E-mail: hanaamohamedfadel@ymail.com
Citation: Fadel HM, Afifi R (2017) Investigation of avian influenza infection in wild birds in Ismailia and Damietta cities, Egypt, Veterinary World, 10(6): 695-701.Aim: This study was carried out to monitor avian influenza (AI) infection in wild birds in Egypt.
Materials and Methods: A total of 135 wild birds were examined for the presence of H5, H7, and H9 hemagglutination inhibition antibodies. Organs and swab samples of 75 birds were screened by multiplex real-time reverse transcriptase-polymerase chain reaction (RRT-PCR) to detect AI subtypes H5, H7, and H9 matrix genes.
Results: The highest seropositive result was recorded in cattle egrets (90.9%) followed by crows (88.6%), semi-captive pigeons (44.8%), and moorhens (39.1%). In cattle egrets, semi-captive pigeons and moorhens, H5 antibodies predominated. In crows, H9 antibodies predominated. Multiple infections with two or three virus subtypes were highest in crows (6/39, 15.4%) followed by cattle egrets (3/30, 10%) and moorhens' (1/9, 11.1%) positive samples. Multiplex RRT-PCR results revealed two positive samples in cattle egrets and moorhens.
Conclusion: The results indicated high seropositive rates against AI virus subtypes H5 and H9 in the examined wild birds. Multiple infections with more than one AI virus (AIV) subtypes were detected in some birds. This requires a collaboration of efforts to monitor AIV infection in wild birds and implement suitable early intervention measures.
Keywords: avian influenza, hemagglutination inhibition, real-time reverse transcriptase-polymerase chain reaction, wild birds.
1. Sorrell, E.M., Wan, H., Araya, Y., Song, H. and Perez, D.R. (2009) Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc. Natl. Acad. Sci. USA., 106(18): 7565-7570. [Crossref] [PubMed] [PMC]
2. Steinhauer, D.A. and Skehel, J.J. (2002) Genetics of influenza viruses. Annu. Rev. Genet., 36: 305-332. [Crossref] [PubMed]
3. Payungporn, S., Chutinimitkul, S., Chaisingh, A., Damrongwantanapokin, S., Nuansrichay, B., Pinyochon, W., Amonsin, A., Donis, R.O., Theamboonlers, A. and Poovorawan, Y. (2006) Discrimination between highly pathogenic and low pathogenic H5 avian influenza A viruses. Emerg. Infect. Dis., 12(4): 700-701. [Crossref] [PubMed] [PMC]
4. Webster, R.G., Bean, W.J., Gorman, O.T., Chambers, T.M. and Kawaoka, Y. (1992) Evolution and ecology of influenza A viruses. Microbiol. Rev., 56(1): 152-179. [PubMed] [PMC]
5. Fouchier, R.A. and Munster, V.J. (2009) Epidemiology of low pathogenic avian influenza viruses in wild birds. Rev. Sci. Tech. Off. Int. Epiz., 28(1): 49-58. [Crossref]
6. Kalthoff, D., Globig, A. and Beer, M. (2010) (Highly pathogenic) avian influenza as a zoonotic agent. Vet. Microbiol., 140(3-4): 237-245. [Crossref] [PubMed]
7. Keawcharoen, J., van den Broek, J., Bouma, A., Tiensin, T., Osterhaus, A.D. and Heesterbeek, H. (2011) Wild Birds and increased transmission of highly pathogenic avian influenza (H5N1) among poultry, Thailand. Emerg. Infect. Dis., 17(6): 1016-1022. [Crossref] [PubMed]
8. William, R.A.J. and Peterson, T.A. (2009) Ecology and geography of avian influenza (HPA1, H5N1) transmission in the Middle East and Northeastern Africa. Int. J. Health Geogr., 8: 47-57. [Crossref] [PubMed] [PMC]
9. Capua, I. and Alexander, D.J. (2007) Animal and health implications of avian influenza infections. Biosci. Rep., 27(6): 359-372. [Crossref] [PubMed]
10. Mase, M., Tsukamoto , K., Imada, T., Imai, K., Tanimura, N,. Nakamura, K., Yamamoto, Y., Hitomi, T., Kira, T., Nakai, T., Kiso, M., Horimoto, T., Kawaoka, Y. and Yamaguchi, S. (2005) Characterization of H5N1 influenza a virus isolated during the 2003-2004 influenza outbreaks in Japan. Virology, 332(1): 167-176. [Crossref] [PubMed]
11. Office International des Epizoties (OIE). (2006) World Animal Health Information Database, Summary of Immediate Notifications and Follow. France: OIE.
12. Sheta, B.M., Fuller, T.L., Larison, B., Niabo, K.Y., Ahmed, A.S., Harrigan, R., Chasar, A., Aziz, S.A., Khidr, A.A., Elbokl, M.M., Habbak, L.Z. and Smith, T.B. (2014) Putative human and avian risk factors for avian influenza virus infections in backyard poultry in Egypt. Vet. Microbiol., 168(1): 208-213. [Crossref] [PubMed] [PMC]
13. Aly, M.M., Arfa, A., Kilany, W.H., Sleim, A.A. and Hassan, M.K. (2010) Isolation of a low pathogenic avian influenza virus (H7N7) from a black kite (Milvus migrans) in Egypt in 2005. Avian Dis., 54(1): 457-460. [Crossref] [PubMed]
14. Soliman, A., Saad, M., Elassal, E., Amir, E., Plathonoff, C., Bahgat, V., Elbadry, M., Ahmed, L.S., Fouda, M., Gamaleldin, M., Mohamed, N., Salyer, S., Cornelius, C. and Barthe, R. (2012) Surveillance of avian influenza viruses in migratory birds in Egypt 2003-09. J. Wildl. Dis., 48(3): 669-675. [Crossref] [PubMed]
15. Arafa, A.S., Haggag, N., Erfan, A., Mady, W., EL-Husseiny, M., Adel, A. and Nasef, S. (2012) Complete genome characterization of avian influenza virus subtypes H9N2 from a commercial quail flock in Egypt. Virus Genes, 45(2): 283-294. [Crossref] [PubMed]
16. Alexander, D.J. (2000) A review of avian influenza in different bird species. Vet. Microbiol., 74: 3-13. [Crossref]
17. Duan, L., Campitelli, L., Fan, X.H., Leung, Y.H.C., Vijakykrishna, D., Zhang, J.X., Donatelli, I., Delogu, M., Li, K.S, Foni, E., Chiapponi, C., Wu, W.L., Kai, H., Webster, R.G., Shortridge, K.F., Peiris, J.S.M., Smith, G.J.D., Chen, H. and Guan, Y. (2007) Characterization of low-pathogenic H5 subtype influenza viruses from Eurasia: Implications for the origin of highly pathogenic H5N1 viruses. J. Virol., 81(14): 7529-7539. [Crossref] [PubMed] [PMC]
18. Hassan, M.K. (2013) Seeking the reasons of avian influenza endemicity in Egypt. [M V Sc Dissertation]. Animal Poultry and Environmental Hygiene, Faculty of Veterinary Medicine, Cairo University, Egypt.
19. Kayali, G., Kandeil, A., El-Shesheny, R., Kayed, A.S., Maatouq, A.M., Cai, Z., McKenzie, P.P., Webby, R.J., El Refaey, S., Kandeel, A. and Ali, M.A. (2016) Avian influenza a (H5N1) virus in Egypt. Emerg. Infect. Dis., 22(3): 379-388. [Crossref] [PubMed] [PMC]
20. Perkins, L.E. and Swayne, D.E. (2003) Comparative susceptibility of selected avian and mammalian species to a Hong Kong-origin H5N1 high-pathogenicity avian influenza virus. Avian Dis., 47: 956-967. [Crossref]
21. AVMA Guidelines on Euthanasia: 2007 Edition. American Veterinary Medical Association, 1931 N Meacham Road Schaumburg, IL, 60173.
22. Office International des Epizoties (OIE). (2008) Highly pathogenic avian influenza. Manual of diagnostic tests and vaccines for terrestrial animals. Available from: http://www.oie.int/fileadmin/home/eng/health-standards/tahm/20304_al pdf. Last accessed on 10-01-2016.
23. Slomka, M.J., Pavlidis, T., Banks, J., Shell, W., McNally, A., Essen, S. and Brown, I.H. (2007) Validated H5 Eurasian real-time reverse transcriptase-polymerase chain reaction and its application in H5N1 outbreaks in 2005-2006. Avian Dis., 51(1): 373-377. [Crossref] [PubMed]
24. Slomka, M.J., Pavlidis, T., Coward, V.J., Voermans, J., Koch, G., Hanna, A., Banks, J. and Brown, I.H. (2009) Validated real time reverse transcriptase PCR methods for the diagnosis and pathotyping of Eurasian H7 avian influenza viruses. Influenza Other Respir Viruses, 3(4): 151-164. [Crossref] [PubMed] [PMC]
25. Ben Shabat, M., Meir, R., Haddas, R., Lapin, E., Shkoda, I., Raibstein, I., Perk, S. and Davidson, I. (2010) Development of a real-time TaqMan RT-PCR assay for the detection of H9N2 avian influenza viruses. J. Virol. Methods, 168(1-2): 72-77. [Crossref] [PubMed]
26. 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]
27. Food and Agriculture Organization of the United Nations (FAO). (2016) Viale delle Terme di Caracalla Rome, Italy. Available from: http://www.fao.org/avianflu/. Last accessed on 15-03-2016.
28. Suliman, A.S., Meier, G.G. and Haverson, P.J. (2011) Eradication of the house crow from Socotra Island, Yemen. In: Veitch, C.R., Clout, M.N. and Towns, D.R., editors . Island invasives: Eradication and management. IUCN, Gland, Switzerland. p361-363.
29. Kamel, A.A. (2014) Potential impacts of invasive house crows (Corvus splendens) bird species in Ismailia Governorate, Egypt; ecology, control and risk management. J. Life Sci. Technol., 2(2): 86-89.
30. Das, B.R., Tosh, C., Kumar, M., Nagaraian, S., Murugkar, H.V., Shukla, S., Tripathi, S., Mishra, A. and Kulkani, D. (2014) Isolation and genetic characterization of influenza a (subtype H5N1) virus from crow in India. Adv. Anim. Vet. Sci., 2(11): 620-624. [Crossref]
31. Khan, S.U., Berman, L., Haider, N., Gerloff, N., Rahman, M.Z., Shu ,B., Rahman, M., Dey, T.K., Davis, T.C., Das, B.C., Balish, A., Islam, A., Teifke, J.P., Zeidner, N., Lindstrom, S., Klimov, A., Donis, R.O., Luby, S.P., Shivaprasad, H.L. and Mikolon, A.B. (2014) Investigating a crow die-off in January-February 2011 during the introduction of a new clade of highly pathogenic avian influenza virus H5N1 into Bangladesh. Arch. Virol., 159(3): 509-518. [Crossref] [PubMed]
32. Xu, K.M., Smith, G.J., Bahl, J., Duan, L., Tai, H., Vijaykrishna, D., Wang, J., Zhang, J.X., Li, K.S., Fan, X.H., Webster, R.G., Chen, H., Peiris, J.S.M. and Guan, Y. (2007) The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J. Virol., 81(19): 10389-10401. [Crossref] [PubMed] [PMC]
33. Sun, Y. and and Liu, J. (2015) H9N2 influenza virus in China: A cause of concern. Protein Cell, 6(1): 18-25. [Crossref] [PubMed]
34. Khawaja, J.Z., Naeem, K., Ahmed, Z. and Ahmed, S. (2005) Surveillance of avian influenza virus in wild birds in areas adjacent to epicenter of an outbreak in federal capital territory of Pakistan. Int. J. Poult. Sci., 4(1): 39-43. [Crossref]
35. Iqbal, M., Yaqub, T., Mukhtar, N., Shabbir, M.Z. and McCauley, J.W. (2013) Infectivity and transmissibility of H9N2 avian influenza virus in chickens and wild terrestrial birds. Vet. Res., 44: 100-109. [Crossref] [PubMed] [PMC]
36. Caron, A., Grosbois, V., Etter, E., Gaidet, N. and de Garine-Wichatitsky, M. (2014) Bridge hosts for avian influenza viruses at the wildlife/domestic interface: An eco-epidemiological framework implemented in Southern Africa. Prev. Vet. Med., 117(3-4): 590-600. [Crossref] [PubMed]
37. Klopfleisch, R.K., Werner, O., Mundt, E.M., Harder, T. and Teifke, J.P. (2006) Neurotropism of highly pathogenic avian influenza virus A/chicken/Indonesia/2003 (H5N1) in experimentally infected pigeons (Columba livia f. domestica). Vet. Pathol., 43(4): 463-470. [Crossref] [PubMed]
38. Mansour, S.M., El-Bakrey, R.M., Ali, H., Knudsen, D.E and Eid, A.A. (2014) Natural infection with highly pathogenic avian influenza virus H5N1 in domestic pigeons (Columba livia) in Egypt. Avian Pathol., 43(4): 319-324. [Crossref] [PubMed]
39. Al-Attar, M.Y., Danial, F.A. and Al-Baroodi, S.Y. (2008) Detection of antibodies against avian influenza virus in wild pigeons and starlings. J. Anim. Vet. Adv., 7(4): 448-449.
40. Perkins, L.E. and Swayne, D.E. (2002) Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks, and pigeons. Avian Dis., 46(1): 53-63. [Crossref]
41. El-Zoghby, E.F., Aly, M.M., Nasef, S.A., Hassan, M.K., Arafa, A.S., Selim, A.A., Kholousy, S.G., Kilany, W.H., Safwat, M., Abdelwhab, E.M. and Hafez, H.M. (2013) Surveillance on A/H5N1 virus in domestic poultry and wild birds in Egypt. Virol. J., 10: 203-212. [Crossref] [PubMed] [PMC]
42. Mehrabanpour, M.J., Rahimian, A., Shirazinezhad, A., Moein, H. and Shayanfar, M.A. (2012) Influenza virus in migratory and resident birds during migratory season in Boushehr, Iran. Turk. J. Vet. Anim. Sci., 36(4): 446-450.
43. El-Zoghby, E.F., Abdelwhab, E.M., Arafa, A., Selim, A.A., Kholousy, S.G., Kilany, W.H., Hassan, M.K., El-Kanawati, Z., Aly, M.M. and Hafez, H.M. (2011) Active surveillance of avian influenza virus in backyard birds in Egypt. J. Appl. Poult. Res., 20(4): 584-588. [Crossref]
44. Saad, M.D., Gamal-Eldein, M.A., Ahmed, L.S., Goda, A.S., Khalil, A.S.A., Fouda, M.A., Yingst, S.L., Parker, M.A. and Montevillel, M.R. (2008) First record of avian influenza (H5N1) in migratory birds in Egypt. Suez Canal Veterinary Medical Journal 13(1): 93-104.