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Insights into the role of turkeys as potential intermediate host for influenza viruses

Published online by Cambridge University Press:  31 August 2016

S.A. ABID ,
T. AZEEM ,
W. AHMAD ,
Z.I. CHAUDHRY  and
S. UMAR
S.A. ABID
Affiliation:
Department of Pathology, University of Veterinary & Animal Sciences Lahore, Pakistan
T. AZEEM
Affiliation:
Department of Pathology, University of Veterinary & Animal Sciences Lahore, Pakistan
W. AHMAD
Affiliation:
Department of Pathology, University of Veterinary & Animal Sciences Lahore, Pakistan
Z.I. CHAUDHRY
Affiliation:
Department of Pathology, University of Veterinary & Animal Sciences Lahore, Pakistan
S. UMAR*
Affiliation:
Department of Pathobiology, PMAS Arid Agriculture University Rawalpindi, Pakistan National Veterinary School of Toulouse, France
*
Corresponding author: sajncvi@gmail.com
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Abstract

Avian influenza viruses have become endemic in land-based domestic poultry and have crossed species barriers. Turkeys are an important host in influenza virus ecology because they are susceptible to infection with these viruses and are often involved in inter species transmission. Several previous studies reveal that waterfowl-origin influenza viruses can be more easily transmitted to domestic turkeys than to chickens. Studies indicate turkeys to be better hosts for low pathogenic avian influenza viruses isolated from commercial poultry operations and live bird markets in comparison to chickens. Moreover, turkeys require low, 50% infectious-dose titres from wild bird as well as poultry adapted viruses, suggesting their high susceptibility for infection following a low dose exposure. Additionally, interspecies transmission of swine influenza viruses to turkeys occurs frequently, thus turkeys may be considered as a bridge species between poultry and wildlife. These findings suggest that turkeys can be easily infected with influenza viruses of different origins and highlight the potential role of turkeys in the transmission and maintenance of influenza viruses between premises.

Keywords

turkeysinfluenza virusesinterspecies transmissionintermediate hosts
Type
Reviews
Information
World's Poultry Science Journal , Volume 72 , Issue 3 , September 2016 , pp. 585 - 596
Copyright
Copyright © World's Poultry Science Association 2016 

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References

ALEXANDER, D. (1982) Isolation of influenza a viruses from birds in great britain during 1980 and 1981. The Veterinary Record 111: 319-321.Google Scholar
ALEXANDER, D., ALLAN, W., PARSONS, D. and PARSONS, G. (1978) The pathogenicity of four avian influenza viruses for fowls, turkeys and ducks. Research in Veterinary Science 24: 242-247.Google Scholar
ALEXANDER, D., PARSONS, G. and MANVELL, R. (1986) Experimental assessment of the pathogenicity of eight avian influenza a viruses of h5 subtype for chickens, turkeys, ducks and quail. Avian Pathology 15: 647-662.Google Scholar
ALI, A., YASSINE, H., AWE, O.O., IBRAHIM, M., SAIF, Y.M. and LEE, C.-W. (2013) Replication of swine and human influenza viruses in juvenile and layer turkey hens. Veterinary Microbiology 163: 71-78.Google Scholar
BROWN, I., LUDWIG, S., OLSEN, C., HANNOUN, C., SCHOLTISSEK, C., HINSHAW, V., HARRIS, P., MCCAULEY, J., STRONG, I. and ALEXANDER, D. (1997) Antigenic and genetic analyses of H1N1 influenza a viruses from european pigs. Journal of General Virology 78: 553-562.Google Scholar
CAMPITELLI, L., MOGAVERO, E., DE MARCO, M.A., DELOGU, M., PUZELLI, S., FREZZA, F., FACCHINI, M., CHIAPPONI, C., FONI, E. and CORDIOLI, P. (2004) Interspecies transmission of an H7N3 influenza virus from wild birds to intensively reared domestic poultry in italy. Virology 323: 24-36.Google Scholar
CHOI, Y.K., LEE, J.H., ERICKSON, G., GOYAL, S.M., JOO, H.S., WEBSTER, R.G. and WEBBY, R.J. (2004) H3N2 influenza virus transmission from swine to turkeys, united states. Emerging Infectious Diseases 10: 2156-2160.Google Scholar
CORRAND, L., DELVERDIER, M., LUCAS, M.N., CROVILLE, G., FACON, C., BALLOY, D., DUCATEZ, M. and GUERIN, J.L. (2012) A low-pathogenic avian influenza H6N1 outbreak in a turkey flock in France: a comprehensive case report. Avian Pathology 41: 569-577.Google Scholar
DEVENTHIRAN, J., KUMAR, S.R., RAGHUNATH, S., LEROITH, T. and ELANKUMARAN, S. (2016) Pb1-f2 protein does not impact the virulence of triple-reassortant H3N2 swine influenza virus in pigs but alters pathogenicity and transmission in turkeys. Journal of Virology 90: 222-231.Google Scholar
FOUCHIER, R.A., MUNSTER, V., WALLENSTEN, A., BESTEBROER, T.M., HERFST, S., SMITH, D., RIMMELZWAAN, G.F., OLSEN, B. and OSTERHAUS, A.D. (2005) Characterization of a novel influenza a virus hemagglutinin subtype (H16) obtained from black-headed gulls. Journal of Virology 79: 2814-2822.Google Scholar
GAGNEUX, P., CHERIYAN, M., HURTADO-ZIOLA, N., VAN DER LINDEN, E.C.B., ANDERSON, D., MCCLURE, H., VARKI, A. and VARKI, N.M. (2003) Human-specific regulation of α2-6-linked sialic acids. Journal of Biological Chemistry 278: 48245-48250.Google Scholar
GAMBARYAN, A., PISKAREV, V., YAMSKOV, I., SAKHAROV, A., TUZIKOV, A., BOVIN, N., NIFANT'EV, N. and MATROSOVICH, M. (1995) Human influenza virus recognition of sialyloligosaccharides. FEBS letters 366: 57-60.Google Scholar
GAMBARYAN, A., WEBSTER, R. and MATROSOVICH, M. (2002) Differences between influenza virus receptors on target cells of duck and chicken. Archives of Virology 147: 1197-1208.Google Scholar
GAMBARYAN, A., YAMNIKOVA, S., LVOV, D., TUZIKOV, A., CHINAREV, A., PAZYNINA, G., WEBSTER, R., MATROSOVICH, M. and BOVIN, N. (2005) Receptor specificity of influenza viruses from birds and mammals: New data on involvement of the inner fragments of the carbohydrate chain. Virology 334: 276-283.Google Scholar
GARCIA, M., CRAWFORD, J.M., LATIMER, J.W., RIVERA-CRUZ, E. and PERDUE, M.L. (1996) Heterogeneity in the haemagglutinin gene and emergence of the highly pathogenic phenotype among recent H5N2 avian influenza viruses from mexico. Journal of General Virology 77: 1493-1504.Google Scholar
GUO, C.T., TAKAHASHI, N., YAGI, H., KATO, K., TAKAHASHI, T., YI, S.-Q., CHEN, Y., ITO, T., OTSUKI, K. and KIDA, H. (2007) The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza a viruses to human type receptors. Glycobiology 17: 713-724.Google Scholar
HALVORSON, D., KELLEHER, C. and SENNE, D. (1985) Epizootiology of avian influenza: Effect of season on incidence in sentinel ducks and domestic turkeys in minnesota. Applied and Environmental Microbiology 49: 914-919.Google Scholar
HIGA, H.H., ROGERS, G.N. and PAULSON, J.C. (1985) Influenza virus hemagglutinins differentiate between receptor determinants bearing n-acetyl-, n-glycollyl-, and n, o-diacetyineuraminic acids. Virology 144: 279-282.Google Scholar
HINSHAW, V., WEBSTER, R., BEAN, W., DOWNIE, J. and SENNE, D. (1983) Swine influenza-like viruses in turkeys: Potential source of virus for humans? Science 220: 206-208.Google Scholar
HUMBERD, J., GUAN, Y. and WEBSTER, R.G. (2006) Comparison of the replication of influenza a viruses in chinese ring-necked pheasants and chukar partridges. Journal of Virology 80: 2151-2161.CrossRefGoogle ScholarPubMed
IMAI, M. and KAWAOKA, Y. (2012) The role of receptor binding specificity in interspecies transmission of influenza viruses. Current opinion in Virology 2: 160-167.CrossRefGoogle ScholarPubMed
ITO, T., SUZUKI, Y., SUZUKI, T., TAKADA, A., HORIMOTO, T., WELLS, K., KIDA, H., OTSUKI, K., KISO, M. and ISHIDA, H. (2000) Recognition of n-glycolylneuraminic acid linked to galactose by the α2, 3 linkage is associated with intestinal replication of influenza a virus in ducks. Journal of Virology 74: 9300-9305.Google Scholar
KAPCZYNSKI, D.R., GONDER, E., LILJEBJELKE, K., LIPPERT, R., PETKOV, D. and TILLEY, B. (2009) Vaccine-induced protection from egg production losses in commercial turkey breeder hens following experimental challenge with a triple-reassortant H3N2 avian influenza virus. Avian Diseases 53: 7-15.Google Scholar
LADMAN, B., ROSENBERGER, S., ROSENBERGER, J., POPE, C. and GELB, J. (Jr) (2008) Virulence of low pathogenicity H7N2 avian influenza viruses from the delmarva peninsula for broiler and leghorn chickens and turkeys. Avian Diseases 52: 623-631.Google Scholar
LEE, C.W., SENNE, D.A., LINARES, J.A., WOOLCOCK, P.R., STALLKNECHT, D.E., SPACKMAN, E., SWAYNE, D.E. and SUAREZ, D.L. (2004) Characterization of recent h5 subtype avian influenza viruses from us poultry. Avian Pathology 33: 288-297.Google Scholar
LIU, M., GUAN, Y., PEIRIS, M., HE, S., WEBBY, R., PEREZ, D. and WEBSTER, R. (2003) The quest of influenza a viruses for new hosts. Avian Diseases 47: 849-856.Google Scholar
MATROSOVICH, M., GAMBARYAN, A., TENEBERG, S., PISKAREV, V., YAMNIKOVA, S., LVOV, D., ROBERTSON, J. and KARLSSON, K.A. (1997) Avian influenza a viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the ha receptor-binding site. Virology 233: 224-234.Google Scholar
MO, I., BRUGH, M., FLETCHER, O., ROWLAND, G. and SWAYNE, D. (1997) Comparative pathology of chickens experimentally inoculated with avian influenza viruses of low and high pathogenicity. Avian Diseases 5: 125-136.Google Scholar
OLSEN, C.W., KARASIN, A.I., CARMAN, S., LI, Y., BASTIEN, N., OJKIC, D., ALVES, D., CHARBONNEAU, G., HENNING, B.M. and LOW, D.E. (2006) Triple reassortant H3N2 influenza a viruses, Canada, 2005. Emerging Infectious Diseases 12: 1132-1135.Google Scholar
PANIGRAHY, B., SENNE, D.A. and PEDERSEN, J.C. (2002) Avian influenza virus subtypes inside and outside the live bird markets, 1993-2000: A spatial and temporal relationship. Avian Diseases 46: 298-307.Google Scholar
PEREZ, D., WEBBY, R., HOFFMANN, E. and WEBSTER, R. (2003) Land-based birds as potential disseminators of avian/mammalian reassortant influenza a viruses. Avian Diseases 47: 1114-1117.Google Scholar
PERKINS, L. and SWAYNE, D. (2001) Pathobiology of a/chicken/hong kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Veterinary Pathology 38: 149-164.Google Scholar
PILLAI, S., PANTIN-JACKWOOD, M., JADHAO, S., SUAREZ, D., WANG, L., YASSINE, H., SAIF, Y. and LEE, C.W. (2009) Pathobiology of triple reassortant h3n2 influenza viruses in breeder turkeys and its potential implication for vaccine studies in turkeys. Vaccine 27: 819-824.Google Scholar
PILLAI, S., PANTIN-JACKWOOD, M., YASSINE, H., SAIF, Y. and LEE, C. (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
SAIF, Y.M., FADLY, A.M., GLISSON, J.R., MCDOUGALD, L.R., NOLAN, L.K. and SWAYNE, D.E. (2008) Diseases of Poultry12th edition. Blackwell Publishers, Iowa, USA: 75-93.Google Scholar
SENNE, D., SUAREZ, D., STALLNECHT, D., PEDERSEN, J. and PANIGRAHY, B. (2005) Ecology and epidemiology of avian influenza in north and south america. Developments in Biologicals 124: 37-44.Google Scholar
SHI, Y., WU, Y., ZHANG, W., QI, J. and GAO, G.F. (2014) Enabling the'host jump': Structural determinants of receptor-binding specificity in influenza a viruses. Nature Reviews Microbiology 12: 822-831.Google Scholar
SHORT, K.R., RICHARD, M., VERHAGEN, J.H., VAN RIEL, D., SCHRAUWEN, E.J.A., VAN DEN BRAND, J.M.A, MÄNZ, B., BODEWEGES, R. and HERFST, S. (2015) One health, multiple challenges: The inter-species transmission of influenza A virus. One Health 1: 1-13.Google Scholar
SLEMONS, R. and SWAYNE, D. (1995) Tissue tropism and replicative properties of waterfowl-origin influenza viruses in chickens. Avian Diseases 39: 521-527.Google Scholar
SOBHANA, R., LAURE, D., ROGERS, C.T., DAN, Q. and ELANKUMARAN, S. (2008) Receptor specificity and host adaptation of recent swine influenza viruses. Proceedings of the 89th Annual meeting of the conference of research workers in animal diseases, CRWAD, Chicago, IL. p. 160.Google Scholar
SPACKMAN, E., SWAYNE, D.E., SUAREZ, D.L., SENNE, D.A., PEDERSEN, J.C., KILLIAN, M.L., PASICK, J., HANDEL, K., PILLAI, S.P.S. and LEE, C.W. (2007) Characterization of low-pathogenicity H5N1 avian influenza viruses from north america. Journal of Virology 81: 11612-11619.Google Scholar
STURM-RAMIREZ, K., HULSE-POST, D., GOVORKOVA, E., HUMBERD, J., SEILER, P., PUTHAVATHANA, P., BURANATHAI, C., NGUYEN, T., CHAISINGH, A. and LONG, H. (2005) Are ducks contributing to the endemicity of highly pathogenic h5n1 influenza virus in asia? Journal of Virology 79: 11269-11279.Google Scholar
SUAREZ, D., WOOLCOCK, P., BERMUDEZ, A. and SENNE, D. (2002) Isolation from turkey breeder hens of a reassortant h1n2 influenza virus with swine, human, and avian lineage genes. Avian Diseases 46: 111-121.Google Scholar
SUAREZ, D.L., GARCIA, M., LATIMER, J., SENNE, D. and PERDUE, M. (1999) Phylogenetic analysis of h7 avian influenza viruses isolated from the live bird markets of the northeast united states. Journal of Virology 73: 3567-3573.Google Scholar
SUZUKI, T., SEKO, A., KITAJIMA, K., INOUE, Y. and INOUE, S. (1993) Identification of peptide: N-glycanase activity in mammalian-derived cultured cells. Biochemical and Biophysical Research Communications 194: 1124-1130.Google Scholar
SWAYNE, D.E. and SLEMONS, R.D. (2008) Using mean infectious dose of high-and low-pathogenicity avian influenza viruses originating from wild duck and poultry as one measure of infectivity and adaptation to poultry. Avian Diseases 52: 455-460.Google Scholar
TANG, Y., LEE, C., ZHANG, Y., SENNE, D., DEARTH, R., BYRUM, B., PEREZ, D., SUAREZ, D. and SAIF, Y. (2005) Isolation and characterization of H3N2 influenza a virus from turkeys. Avian Diseases 49: 207-213.Google Scholar
TONG, S., ZHU, X., LI, Y., SHI, M., ZHANG, J., BOURGEOIS, M., YANG, H., CHEN, X., RECUENCO, S. and GOMEZ, J. (2013) New world bats harbor diverse influenza a viruses. PLoS Pathogen 9: e1003657.Google Scholar
TUMPEY, T.M., KAPCZYNSKI, D.R. and SWAYNE, D.E. (2004) Comparative susceptibility of chickens and turkeys to avian influenza a H7N2 virus infection and protective efficacy of a commercial avian influenza H7N2 virus vaccine. Avian Diseases 48: 167-176.Google Scholar
ULLAH, S., RIAZ, N., SHAH, M.A.A. and UMAR, S. (2013) DNA vaccines against avian influenza: current research and future prospects. World's Poultry Science Journal 69: 125-134.Google Scholar
UMAR, S., REHMAN, A., YOUNUS, M., SHAHZAD, M., NISA, Q., YAQOOB, M. and SHAH, M.A.A. (2015a) Effects of Nigella sativa on immune responses and pathogenesis of avian influenza (H9N2) virus in turkeys; Journal of Applied Poultry Research 25: 95-103.Google Scholar
UMAR, S., YOUNUS, M., REHMAN, M.U., ASLAM, A., SHAH, M.A.A., MUNIR, M.T., HUSSAIN, S., IQBAL, F., FIAZ, M. and ULLAH, S. (2015b) Role of aflatoxin toxicity on transmissibility and pathogenicity of H9N2 avian influenza virus in turkeys. Avian Pathology 44: 305-310.Google Scholar
UMAR, S., SARFRAZ, S., MUSHTAQ, A. and ATTIQUE, M. (2016a) Emerging threat of H9N2 viruses in poultry of pakistan and vaccination strategy. World's Poultry Science Journal 72: 343-352.CrossRefGoogle Scholar
UMAR, S., REHMAN, A., ASIF, S., USMAN, M., ATIF, M., ALI, S., MUNIR, M.T., ALI, A., SHAHZAD, M. and SHAH, M.A.A. (2016b) Variation in viral shedding patterns between domestic and wild terrestrial birds infected experimentally with reassortant avian influenza virus (H9N2). Avian Biology Research(in press).Google Scholar
UMAR, S., KABOUDI, K., BOUZOUAIA, M., MUNIR, M.T., YOUNUS, M., NISA, Q., SHAH, M.A.A., YAQOOB, M. and FIAZ, M. (2016c) Synergistic effects of thymoquinone and curcumin on immune response and anti-viral activity against avian influenza virus (H9N2) in turkeys Poultry Science 95 (7): 1513-1520 doi:10.3382/ps/pew069.Google Scholar
WEBBY, R.J., WOOLCOCK, P.R., KRAUSS, S.L. and WEBSTER, R.G. (2002) Reassortment and interspecies transmission of north american H6N2 influenza viruses. Virology 295: 44-53.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
YASSINE, H.M., LEE, C.-W. and SAIF, Y.M. (2013) Interspecies transmission of influenza a viruses between swine and poultry. Current Topics in Microbiology and Immunology 370: 227-240.Google Scholar
ZANELLA, A., DALL'ARA, P. and MARTINO, P. (2001) Avian influenza epidemic in italy due to serovar H7N1. Avian Diseases 45: 257-261.Google Scholar
ZHOU, N.N., SENNE, D.A., LANDGRAF, J.S., SWENSON, S.L., ERICKSON, G., ROSSOW, K., LIU, L., YOON, K.J., KRAUSS, S. and WEBSTER, R.G. (1999) Genetic reassortment of avian, swine, and human influenza a viruses in american pigs. Journal of Virology 73: 8851-8856.Google Scholar