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Factors responsible for the continuous persistence and evolution of low pathogenic avian influenza virus (H9N2)

Published online by Cambridge University Press:  16 October 2017

M. UMER ASHRAF
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
M. SHAHID MAHMOOD*
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
A. RAFIQUE
Affiliation:
Department of Zoology, GC University, Faisalabad, Pakistan
R. ZAHID ABBAS
Affiliation:
Department of Parasitology, University of Agriculture, Faisalabad, Pakistan
Z. IQBAL
Affiliation:
Department of Parasitology, University of Agriculture, Faisalabad, Pakistan
M. YOUNAS
Affiliation:
CVAS, Jhang, Pakistan
S. AHMAD SADIQ
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
M. USMAN
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
M. OMER ASGHAR
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
M. USMAN ISHAQ
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
*
Corresponding author: shahiduaf@gmail.com
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Abstract

Avian influenza virus (AIV) type A subtype H9N2 usually causes mild asymptomatic infections, and is mostly undetected and is, therefore, under-reported. This has allowed the virus to rapidly evolve via mutations and reassortments in its genome with other avian influenza subtypes especially H1N1, H5N1 and H7N3 thereby introducing new variant strains and producing severe disease. It has been reported that the AIV H9N2 donated its internal genes for the devastating 1997 Hong Kong outbreak and furthermore, it may be the cause of the next influenza pandemic. There are many factors such as its wide host range, ability to cross the species barrier, ecological diversity, antiviral resistance and zoonotic importance that make it an excellent candidate for the next influenza pandemic. These and other factors like ineffective vaccination, negative immunological pressures, lack of surveillance, which contribute to its continuous persistence and evolutionary dynamics are discussed in this paper. It is important to take the necessary measures to control and prevent its unchecked circulation to prevent the future outbreaks.

Type
Reviews
Copyright
Copyright © World's Poultry Science Association 2017 

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References

ABDEL-MONEIM, A.S., AFIFI, M.A. and EL-KADY, M.F. (2012) Isolation and mutation trend analysis of influenza A virus subtype H9N2 in Egypt. Virology Journal 9: 173.Google Scholar
ALEXANDER, D.J. (2000) A review of avian influenza in different bird species. Veterinary Microbiology 74: 3-13.Google Scholar
ALEXANDER, D.J. (2007) An overview of the epidemiology of avian influenza. Vaccine 25: 5637-5644.Google Scholar
ALI, A., SIDDIQUE, N., ABBAS, M.A., GHAFAR, A., RAFIQUE, S., ALI, R., MEMON, A.U.R. and NAEEM, K. (2015) Role of Mannheimia (Pasteurella) haemolytica in Severe Respiratory Tract Infection in Commercial Poultry in Pakistan. Pakistan Veterinary Journal 35: 279-282.Google Scholar
BACHAYA, H.A., ABBAS, R.Z., RAZA, M.A. IQBAL, Z., REHMAN, T.U., BABER, W. and HUSSAIN, R. (2015) Existence of coccidiosis and associated risk factors in broiler chickens in Southern Punjab, Pakistan. Pakistan Veterinary Journal 35: 81-84.Google Scholar
BANET-NOACH, C., PERK, S., SIMANOV, L., GREBENYUK, N., ROZENBLUT, E., POKAMUNSKI, S., PIRAK, M., TENDLER, Y. and PANSHIN, A. (2007) H9N2 influenza viruses from Israeli poultry: a five-year outbreak. Avian Diseases 51: 290-296.Google Scholar
BANKS, J., SPEIDEL, E.C., HARRIS, P.A. and ALEXANDER, D.J. (2000) Phylogenetic analysis of influenza A viruses of H9 haemaglutinin subtype. Avian pathology: Journal of the World Veterinary Poultry Association (W.V.P.A) 29: 353-359.Google Scholar
CARON, A., GAIDET, N., DE GARINE-WICHATITSKY, M., MORAND, S. and CAMERON, E.Z. (2009) Evolutionary biology, community ecology and avian influenza research. Infection, Genetics and Evolution 9: 298-303.Google Scholar
CHEEMA, B.F., SIDDIQUE, M., SHARIF, A., MANSOOR, M.K. and IQBAL, Z. (2011) Sero-prevalence of avian influenza in broiler flocks in district Gujranwala (Pakistan). International Journal of Agriculture and Biology 13: 850-856.Google Scholar
CHEN, L., JIANG, T., LI, X., WANG, Q., WANG, Y. and LI, Y. (2016) Immunomodulatory Activity of β-glucan and Mannan-Oligosaccharides from Saccharomyces cerevisiae on Broiler Chickens Challenged with Feed-Borne Aspergillus fumigatus . Pakistan Veterinary Journal 36: 297-301.Google Scholar
CONG, Y.L., PU, J., LIU, Q.F., WANG, S., ZHANG, G.Z., ZHANG, X.L., FAN, W.X., BROWN, E.G. and LIU, J.H. (2007) Antigenic and genetic characterization of H9N2 swine influenza viruses in China. Journal of General Virology 88: 2035-2041.Google Scholar
CUI, N., LI, Y., SU, S., CUI, Z., DING, J., KANG, M., SUN, P. and ZHU, H. (2016) Protection of chickens against very virulent Marek's Disease Virus (MDV) by an infectious clone of Meq-null MDV vaccination. Pakistan Veterinary Journal 36: 16-20.Google Scholar
DOMINGO, E., MARTÍNEZ-SALAS, E., SOBRINO, F., DE LA TORRE, J.C., PORTELA, A., ORTÍN, J., LÓPEZ-GALINDEZ, C., PÉREZ-BREÑA, P., VILLANUEVA, N., NÁJERA, R., VANDEPOL, S., STEINHAUER, D., DEPOLO, N. and HOLLAND, J. (1985) The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance - a review. Gene 40: 1-8.Google Scholar
DONG, G., LUO, J., ZHANG, H., WANG, C., DUAN, M., DELIBERTO, T.J., NOLTE, D.L., JI, G. and HE, H. (2011) Phylogenetic diversity and genotypical complexity of H9N2 influenza A viruses revealed by genomic sequence analysis. PLoS ONE 6.Google Scholar
ESCORCIA, M., VÁZQUEZ, L., MÉNDEZ, S.T., RODRÍGUEZ-ROPÓN, A., LUCIO, E. and NAVA, G.M. (2008) Avian influenza: genetic evolution under vaccination pressure. Virology Journal 5: 15.Google Scholar
GAO, H., XU, G., SUN, Y., QI, L., WANG, J., KONG, W., SUN, H., PU, J., CHANG, K. C. and LIU, J. (2015) PA-X is a virulence factor in avian H9N2 influenza virus. Journal of General Virology 96: 2587-2594.Google Scholar
GE, F.F., ZHOU, J.P., LIU, J., WANG, J., ZHANG, W.Y., SHENG, L.P., XU, F., JU, H.B., SUN, Q.Y. and LIU, P.H. (2009) Genetic evolution of H9 subtype influenza viruses from live poultry markets in Shanghai, China. Journal of Clinical Microbiology 47: 3294-3300.Google Scholar
GUO, Y.J., KRAUSS, S., SENNE, D.A., MO, I.P., LO, K.S., XIONG, X.P., NORWOOD, M., SHORTRIDGE, K.F., WEBSTER, R.G. and GUAN, Y. (2000) Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology 267: 279-88.CrossRefGoogle ScholarPubMed
HADIPOUR, M.M. (2010) Seroprevalence survey of H9N2 avian influenza virus in backyard chickens around the Caspian Sea in Iran. Brazilian Journal of Poultry Science 12: 53-55.Google Scholar
HATTA, M., GAO, P., HALFMANN, P. and KAWAOKA, Y. (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science (New York, N.Y.) 293: 1840-1842.Google Scholar
HAY, A.J., ZAMBON, M.C., WOLSTENHOLME, A.J., SKEHEL, J.J. and SMITH, M.H. (1986) Molecular basis of resistance of influenza A viruses to amantadine. The Journal of Antimicrobial Chemotherapy 18 Suppl B: 19-29.Google Scholar
HULSE, D.J., WEBSTER, R.G., RUSSELL, R.J. and PEREZ, D.R. (2004) Molecular determinants within the surface proteins involved in the pathogenicity of H5N1 influenza viruses in chickens. Journal of Virology 78: 9954.Google Scholar
KAMMON, A., HEIDARI, A., DAYHUM, A., ELDAGHAYES, I., SHARIF, M., MONNE, I., CATTOLI, G., ASHEG, A., FARHAT, M. and KRAIM, E. (2015) Characterization of Avian Influenza and Newcastle Disease Viruses from Poultry in Libya. Avian Diseases 59: 422-430.Google Scholar
KISHIDA, N., SAKODA, Y., ETO, M., SUNAGA, Y. and KIDA, H. (2004) Co-infection of Staphylococcus aureus or Haemophilus paragallinarum exacerbates H9N2 influenza A virus infection in chickens. Archives of Virology 149: 2095-2104.Google Scholar
LEE, C.-W., SENNE, D.A. and SUAREZ, D.L. (2004) Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. Journal of Virology 78: 8372-81.Google Scholar
LI, C., YU, K., TIAN, G., YU, D., LIU, L., JING, B., PING, J. and CHEN, H. (2005) Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology 340: 70-83.Google Scholar
LIN, Y.P., SHAW, M., GREGORY, V., CAMERON, K., LIM, W., KLIMOV, A., SUBBARAO, K., GUAN, Y., KRAUSS, S., SHORTRIDGE, K., WEBSTER, R., COX, N. and HAY, A. (2000) Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proceedings of the National Academy of Sciences of the United States of America 97: 9654-9658.Google Scholar
LIU, D., SHI, W., SHI, Y., WANG, D., XIAO, H., LI, W., BI, Y., WU, Y., LI, X., YAN, J., LIU, W., ZHAO, G., YANG, W., WANG, Y., MA, J., SHU, Y., LEI, F. and GAO, G.F. (2013) Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. The Lancet 381: 1926-1932.Google Scholar
MA, J., YU, Y., ZHANG, H., MO, H., OU, C., WANG, X. and LIU, X. (2016) Over-expression of Rab1 Gene during Infectious Bursal Disease Virus infection in layer chicken. Pakistan Veterinary Journal 36: 73-76.Google Scholar
MANVELL, R.J., MCKINNEY, P., WERNERY, U. and FROST, K. (2000) Isolation of a highly pathogenic influenza A virus of subtype H7N3 from a peregrine falcon (Falco peregrinus). Avian Pathology 29: 635-637.Google Scholar
MATROSOVICH, M.N., KRAUSS, S. and WEBSTER, R.G. (2001) H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281: 156-162.CrossRefGoogle ScholarPubMed
MOK, C.K., YEN, H.L., YU, M.Y., YUEN, K.M., SIA, S.F., CHAN, M.C., QIN, G., TU, W.W. and PEIRIS, J.S. (2011) Amino acid residues 253 and 591 of the PB2 protein of avian influenza virus A H9N2 contribute to mammalian pathogenesis. Journal of Virology 85: 9641-9645.CrossRefGoogle ScholarPubMed
NILI, H. and ASASI, K. (2003) Avian influenza (H9N2) outbreak in Iran. Avian Diseases 47: 828-831.Google Scholar
OLSEN, B., MUNSTER, V.J., WALLENSTEN, A., WALDENSTRÖM, J., OSTERHAUS, A.D.M.E. and FOUCHIER, R.A.M. (2006) Global patterns of influenza A virus in wild birds. Science (New York, N.Y.) 312: 384-388.Google Scholar
PEIRIS, M., YAM, W.C., CHAN, K.H., GHOSE, P. and SHORTRIDGE, K.F. (1999b) Influenza A H9N2: Aspects of laboratory diagnosis. Journal of Clinical Microbiology 37: 3426-3427.Google Scholar
PEIRIS, M., YUEN, K.Y., LEUNG, C.W., CHAN, K.H., IP, P.L.S., LAI, R.W.M., ORR, W.K. and SHORTRIDGE, K.F. (1999a) Human infection with influenza H9N2. The Lancet 354: 916-917.Google Scholar
PEREZ, D.R., LIM, W., SEILER, J.P., YI, G., PEIRIS, M., SHORTRIDGE, K.F. and WEBSTER, R.G. (2003) Role of quail in the interspecies transmission of H9 influenza A viruses: molecular changes on HA that correspond to adaptation from ducks to chickens. Journal of Virology 77: 3148-3156.Google Scholar
PILLAI, S.P.S., PANTIN-JACKWOOD, M., YASSINE, H.M., SAIF, Y.M. and LEE, C.W. (2010) The high susceptibility of turkeys to influenza viruses of different origins implies their importance as potential intermediate hosts. Avian diseases 54: 522-526.Google Scholar
RAZA, A., AHMAD, A., RABBANI, M., MAHMOOD, A., YOUNUS, M., ALI, Z. and AHAD, A. (2016) . Optimization of quality control factors for indigenous Mycoplasma gallisepticum bacterin preparation and their impact on immunoprophylaxis in broilers. Pakistan Veterinary Journal 36: 227-229.Google Scholar
REED, K.D., MEECE, J.K., HENKEL, J.S. and SHUKLA, S.K. (2003) Birds, Migration and Emerging Zoonoses: West Nile Virus, Lyme Disease, Influenza A and Enteropathogens. Clinical Medicine & Research 1: 5-12.Google Scholar
ROUSSAN, D.A., KHAWALDEH, G.Y., AL RIFAI, R.H., TOTANJI, W.S. and SHAHEEN, I.A. (2009) Avian influenza virus H9 subtype in poultry flocks in Jordan. Preventive Veterinary Medicine 88: 77-81.Google Scholar
SCHNELL, J.R. and CHOU, J.J. (2008) Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451: 591-595.Google Scholar
SEIFI, S., ASASI, K. and MOHAMMADI, A. (2010) Natural co-infection caused by avian influenza H9 subtype and infectious bronchitis viruses in broiler chicken farms. Veterinarski Arhiv 80: 269-281.Google Scholar
SEO, S.H., HOFFMANN, E. and WEBSTER, R.G. (2004) RETRACTED: The NS1 gene of H5N1 influenza viruses circumvents the host anti-viral cytokine responses. Virus Research 103: 107-113.Google Scholar
SIDDIQUE, N., NAEEM, K., AHMED, Z., ABBAS, M.A., ALI, A., RAFIQUE, S., RASHID, F., BEGUM, I. and FAROOQ, R. (2016) Isolation and Sequence Analysis of Reassortant Low Pathogenic Avian Influenza Virus H4N6 from Duck and Chicken in Live Bird Markets from Pakistan. Pakistan Veterinary Journal 36: 258-263.Google Scholar
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. Proceedings of the National Academy of Sciences of the United States of America 106: 7565-7570.Google Scholar
STECH, J., XIONG, X., SCHOLTISSEK, C. and WEBSTER, R.G. (1999) Independence of evolutionary and mutational rates after transmission of avian influenza viruses to swine. Journal of Virology 73: 1878-1884.Google Scholar
SUAREZ, D.L. (2000) Evolution of avian influenza viruses. Veterinary Microbiology 74: 15-27.Google Scholar
SUBBARAO, K. and KATZ, J. (2000) Avian influenza viruses infecting humans. Cellular and Molecular Life Sciences: CMLS 57: 1770-1784.Google Scholar
SUN, Y., PU, J., FAN, L., SUN, H., WANG, J., ZHANG, Y., LIU, L. and LIU, J. (2012) Evaluation of the protective efficacy of a commercial vaccine against different antigenic groups of H9N2 influenza viruses in chickens. Veterinary Microbiology 156: 193-199.Google Scholar
SUN, Y., PU, J., JIANG, Z., GUAN, T., XIA, Y., XU, Q., LIU, L., MA, B., TIAN, F., BROWN, E.G. and LIU, J. (2010) Genotypic evolution and antigenic drift of H9N2 influenza viruses in China from 1994 to 2008. Veterinary Microbiology 146: 215-225.CrossRefGoogle Scholar
THOMPSON, C.I., BARCLAY, W.S. and ZAMBON, M.C. (2004) Changes in in vitro susceptibility of influenza A H3N2 viruses to a neuraminidase inhibitor drug during evolution in the human host. Journal of Antimicrobial Chemotherapy 53: 759-765.Google Scholar
WANG, Q., JU, L., LIU, P., ZHOU, J., LV, X., LI, L., SHEN, H., SU, H., JIANG, L. and JIANG, Q. (2015) Serological and Virological Surveillance of Avian Influenza A Virus H9N2 Subtype in Humans and Poultry in Shanghai, China, Between 2008 and 2010. Zoonoses and Public Health 62: 131-140.Google Scholar
WEBSTER, R.G., BEAN, W.J., GORMAN, O.T., CHAMBERS, T.M. and KAWAOKA, Y. (1992) Evolution and ecology of influenza A viruses. Microbiological Reviews 56: 152-179.Google Scholar
XING, Z., HARPER, R., ANUNCIACION, J., YANG, Z., GAO, W., QU, B., GUAN, Y. and CARDONA, C.J. (2010) Host immune and apoptotic responses to avian influenza virus H9N2 in human tracheobronchial epithelial cells. American Journal of Respiratory Cell and Molecular Biology 44: 24-33.Google Scholar
XU, K.M., SMITH, G.J.D., 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. Journal of Virology 81: 10389-10401.Google Scholar
YU, H., HUA, R.H., WEI, T.C., ZHOU, Y.J., TIAN, Z.J., LI, G.X., LIU, T.Q. and TONG, G.Z. (2008) Isolation and genetic characterization of avian origin H9N2 influenza viruses from pigs in China. Veterinary Microbiology 131: 82-92.Google Scholar