Abstract
The special susceptibility of pigs to infection with avian and mammalian influenza viruses, the close proximity of pigs and poultry farms, and applied human practices in raising and trading of farm animals/farm animal products, provide opportunities for genetic exchange and interspecies transmission of influenza A viruses. Although only H1 and H3 influenza subtypes have widely circulated and caused disease in pig populations worldwide, H9 subtype is being continuously detected in pigs in Asia, plus sporadic infections with highly pathogenic H5-avian influenza viruses. On the other hand, swine viruses are continuously isolated from poultry species, especially turkeys, causing economic losses in poultry production. The viral and host factors contributing to influenza transmission between pigs and poultry are poorly defined. In addition, surveillance programs for influenza viruses in both species, especially pigs, are rarely implemented, and thus, leaving many questions about influenza unanswered. In this review, we summarize early and recent findings about influenza transmission between swine and poultry with emphasis on the role of turkeys.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aamir UB, Naeem K, Ahmed Z, Obert CA, Franks J, Krauss S, Seiler P, Webster RG (2009) Zoonotic potential of highly pathogenic avian H7N3 influenza viruses from Pakistan. Virology 390(2):212–220
Alexander DJ (2007) An overview of the epidemiology of avian influenza. Vaccine 25(30):5637–5644
Aly MM, Arafa A, Hassan MK (2008) Epidemiological findings of outbreaks of disease caused by highly pathogenic H5N1 avian influenza virus in poultry in Egypt during 2006. Avian Dis 52(2):269–277
AVMA (2010) 2009 H1N1 Flu Virus Outbreak. In Public Health, http://www.avma.org/public_health/influenza/new_virus/default.asp.
Beaudoin A, Gramer M, Gray GC, Capuano A, Setterquist S, Bender J (2010) Serologic survey of swine workers for exposure to H2N3 swine influenza A. Influenza Other Respir Viruses 4(3):163–170
Berhane Y, Hisanaga T, Kehler H, Neufeld J, Manning L, Argue C, Handel K, Hooper-McGrevy K, Jonas M, Robinson J, Webster RG, Pasick J (2009) Highly pathogenic avian influenza virus A (H7N3) in domestic poultry, Saskatchewan, Canada, 2007. Emerg Infect Dis 15(9):1492–1495
Brown IH (2008) The role of pigs in interspecies transmission. Monoger Virol Basel, Karger
Brown IH, Banks J, Manvell RJ, Essen SC, Shell W, Slomka M, Londt B, Alexander DJ (2006) Recent epidemiology and ecology of influenza A viruses in avian species in Europe and the Middle East. Dev Biol (Basel) 124:45–50
Campitelli L, Fabiani C, Puzelli S, Fioretti A, Foni E, De Marco A, Krauss S, Webster RG, Donatelli I (2002) H3N2 influenza viruses from domestic chickens in Italy: an increasing role for chickens in the ecology of influenza? J Gen Virol 83(Pt 2):413–420
Castrucci MR, Campitelli L, Ruggieri A, Barigazzi G, Sidoli L, Daniels R, Oxford JS, Donatelli I (1994) Antigenic and sequence analysis of H3 influenza virus haemagglutinins from pigs in Italy. J Gen Virol 75(Pt 2):371–379
Castrucci MR, Donatelli I, Sidoli L, Barigazzi G, Kawaoka Y, Webster RG (1993) Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology 193(1):503–506
Cauthen AN, Swayne DE, Schultz-Cherry S, Perdue ML, Suarez DL (2000) Continued circulation in China of highly pathogenic avian influenza viruses encoding the hemagglutinin gene associated with the 1997 H5N1 outbreak in poultry and humans. J Virol 74(14):6592–6599
Choi YK, Lee JH, Erickson G, Goyal SM, Joo HS, Webster RG, Webby RJ (2004) H3N2 influenza virus transmission from swine to turkeys, United States. Emerg Infect Dis 10(12):2156–2160
Choi YK, Nguyen TD, Ozaki H, Webby RJ, Puthavathana P, Buranathal C, Chaisingh A, Auewarakul P, Hanh NT, Ma SK, Hui PY, Guan Y, Peiris JS, Webster RG (2005) Studies of H5N1 influenza virus infection of pigs by using viruses isolated in Vietnam, Thailand in 2004. J Virol 79(16):10821–10825
Cong YL, Pu J, Liu QF, Wang S, Zhang GZ, Zhang XL, Fan WX, Brown EG, Liu JH (2007) Antigenic and genetic characterization of H9N2 swine influenza viruses in China. J Gen Virol 88(Pt 7):2035–2041
Cong YL, Wang CF, Yan CM, Peng JS, Jiang ZL, Liu JH (2008) Swine infection with H9N2 influenza viruses in China in 2004. Virus Genes 36(3):461–469
de Jong MC, Stegeman A, van der Goot J, Koch G (2009) Intra-and interspecies transmission of H7N7 highly pathogenic avian influenza virus during the avian influenza epidemic in The Netherlands in 2003. Rev Sci Tech 28(1):333–340
El-Sayed A, Awad W, Fayed A, Hamann HP, Zschock M (2010) Avian influenza prevalence in pigs, Egypt. Emerg Infect Dis 16(4):726–727
Gibbs AJ, Armstrong JS, Downie JC (2009) From where did the 2009 ‘swine-origin’ influenza A virus (H1N1) emerge? Virol J 6:207
Halvorson DA, Kelleher CJ, Senne DA (1985) Epizootiology of avian influenza: effect of season on incidence in sentinel ducks and domestic turkeys in Minnesota. Appl Environ Microbiol 49(4):914–919
Hinshaw VS, Webster RG, Bean WJ, Downie J, Senne DA (1983) Swine influenza-like viruses in turkeys: potential source of virus for humans? Science 220(4593):206–208
Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y (1998) Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 72(9):7367–7373
Jung K, Song DS, Kang BK, Oh JS, Park BK (2007) Serologic surveillance of swine H1 and H3 and avian H5 and H9 influenza A virus infections in swine population in Korea. Prev Vet Med 79(2–4):294–303
Kapczynski DR, Gonder E, Liljebjelke K, Lippert R, Petkov D, 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 Dis 53(1):7–15
Karasin AI, Brown IH, Carman S, Olsen CW (2000a) Isolation and characterization of H4N6 avian influenza viruses from pigs with pneumonia in Canada. J Virol 74(19):9322–9327
Karasin AI, Olsen CW, Brown IH, Carman S, Stalker M, Josephson G (2000b) H4N6 influenza virus isolated from pigs in Ontario. Can Vet J 41(12):938–939
Lipatov AS, Kwon YK, Sarmento LV, Lager KM, Spackman E, Suarez DL, Swayne DE (2008) Domestic pigs have low susceptibility to H5N1 highly pathogenic avian influenza viruses. PLoS Pathog 4(7):e1000102
Liu D, Liu X, Yan J, Liu WJ, Gao GF (2009) Interspecies transmission and host restriction of avian H5N1 influenza virus. Sci China C Life Sci 52(5):428–438
Loeffen W, De Boer-Luijtze EA, Koch G (2004) Transmission of highly pathogenic avian influenza virus to swine in Netherlands. In Congress of the international society for Animal Hygiene, 329–330 St. Malo, France: animal production in Europe: the way forward in a changing world
Ma W, Vincent AL, Gramer MR, Brockwell CB, Lager KM, Janke BH, Gauger PC, Patnayak DP, Webby RJ, Richt JA (2007) Identification of H2N3 influenza A viruses from swine in the United States. Proc Natl Acad Sci U S A 104(52):20949–20954
Mohan R, Saif YM, Erickson GA, Gustafson GA, Easterday BC (1981) Serologic and epidemiologic evidence of infection in turkeys with an agent related to the swine influenza virus. Avian Dis 25(1):11–16
Munster VJ, de Wit E, van Riel D, Beyer WE, Rimmelzwaan GF, Osterhaus AD, Kuiken T, Fouchier RA (2007) The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J Infect Dis 196(2):258–265
Neumann G, Chen H, Gao GF, Shu Y, Kawaoka Y (2010) H5N1 influenza viruses: outbreaks and biological properties. Cell Res 20(1):51–61
Ninomiya A, Takada A, Okazaki K, Shortridge KF, Kida H (2002) Seroepidemiological evidence of avian H4, H5, and H9 influenza A virus transmission to pigs in southeastern China. Vet Microbiol 88(2):107–114
Olsen CW (2002) The emergence of novel swine influenza viruses in North America. Virus Res 85(2):199–210
Olsen CW, Karasin A, Erickson G (2003) Characterization of a swine-like reassortant H1N2 influenza virus isolated from a wild duck in the United States. Virus Res 93(1):115–121
Pantin-Jackwood M, Wasilenko JL, Spackman E, Suarez DL, Swayne DE (2010) Susceptibility of turkeys to pandemic-H1N1 virus by reproductive tract insemination. Virol J 7(1):27
Peiris JS, Guan Y, Markwell D, Ghose P, Webster RG, Shortridge KF (2001) Cocirculation 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
Pereda A, Cappuccio J, Quiroga MA, Baumeister E, Insarralde L, Ibar M, Sanguinetti R, Cannilla ML, Franzese D, Cabrera OEE, Craig MI, Rimondi A, Machuca M, Debenedetti RT, Zenobi C, Barral L, Balzano R, Capalbo S, Risso A, Perfumo CJ (2010) Pandemic (H1N1) 2009 Outbreak on a pig farm, Argentina. Emerging infectious diseases: http://www.cdc.gov/eid/content/16/12/pdfs/09-1230.pdf.
Pillai SP, Lee CW (2010) Species and age related differences in the type and distribution of influenza virus receptors in different tissues of chickens, ducks and turkeys. Virol J 7(1):5
Pillai SP, Pantin-Jackwood M, Yassine HM, Saif YM, Lee CW (2010) The high susceptibility of turkeys to influenza viruses of different origins implies their importance as potential intermediate hosts. Avian Dis 54(Suppl 1):522–526
Ramakrishnan MA, Wang P, Abin M, Yang M, Goyal SM, Gramer MR, Redig P, Fuhrman MW, Sreevatsan S (2010) Triple reassortant swine influenza A (H3N2) virus in waterfowl. Emerg Infect Dis 16(4):728–730
Russell C, Hanna A, Barrass L, Matrosovich M, Nunez A, Brown IH, Choudhury B, Banks J (2009) Experimental infection of turkeys with pandemic (H1N1) 2009 influenza virus (A/H1N1/09v). J Virol 83(24):13046–13047
Scholtissek C, Burger H, Bachmann PA, Hannoun C (1983) Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. Virology 129(2):521–523
Shope RE (1931a) The etiology of swine influenza. Science 73(1886):214–215
Shope RE (1931b) Swine influenza : Iii. Filtration experiments and etiology. J Exp Med 54(3):373–385
Sorrell EM, Ramirez-Nieto GC, Gomez-Osorio IG, Perez DR (2007) Genesis of pandemic influenza. Cytogenet Genome Res 117(1–4):394–402
Stegeman A, Bouma A, Elbers AR, de Jong MC, Nodelijk G, de Klerk F, Koch G, van Boven M (2004) Avian influenza A virus (H7N7) epidemic in The Netherlands in 2003: course of the epidemic and effectiveness of control measures. J Infect Dis 190(12):2088–2095
Suarez DL, Woolcock PR, Bermudez AJ, Senne DA (2002) Isolation from turkey breeder hens of a reassortant H1N2 influenza virus with swine, human, and avian lineage genes. Avian Dis 46(1):111–121
Subbaroa K, Swayne D, Olsen CW (2006) Epidemiology and control of human and animal influenza. Caister Academic Press, Norfolk
Swayne DE, Halverson DA (2007) Diseases of poultry: influenza. Blackwell Publishing Professional, Ames
Swayne DE, Pantin-Jackwood M, Kapczynski D, Spackman E, Suarez DL (2009) Susceptibility of poultry to pandemic (H1N1) 2009 Virus. Emerg Infect Dis 15(12):2061–2063
Swayne DE, Radin MJ, Hoepf TM, Slemons RD (1994) Acute renal failure as the cause of death in chickens following intravenous inoculation with avian influenza virus A/chicken/Alabama/7395/75 (H4N8). Avian Dis 38(1):151–157
Tang Y, Lee CW, Zhang Y, Senne DA, Dearth R, Byrum B, Perez DR, Suarez DL, Saif YM (2005) Isolation and characterization of H3N2 influenza A virus from turkeys. Avian Dis 49(2):207–213
Terregino C, De Nardi R, Nisi R, Cilloni F, Salviato A, Fasolato M, Capua I (2009) Resistance of turkeys to experimental infection with an early 2009 Italian human influenza A(H1N1)v virus isolate. Euro Surveill 14(41):19360
Thomas C, Manin TB, Andriyasov AV, Swayne DE (2008) Limited susceptibility and lack of systemic infection by an H3N2 swine influenza virus in intranasally inoculated chickens. Avian Dis 52(3):498–501
Vincent AL, Ma W, Lager KM, Janke BH, Richt JA (2008) Swine influenza viruses a North American perspective. Adv Virus Res 72:127–154
Wood GW, Banks J, Brown IH, Strong I, Alexander DJ (1997) The nucleotide sequence of the HA1 of the haemagglutinin of an HI avian influenza virus isolate from turkeys in Germany provides additional evidence suggesting recent transmission from pigs. Avian Pathol 26(2):347–355
Wright SM, Kawaoka Y, Sharp GB, Senne DA, Webster RG (1992) Interspecies transmission and reassortment of influenza A viruses in pigs and turkeys in the United States. Am J Epidemiol 136(4):488–497
Xu C, Fan W, Wei R, Zhao H (2004) Isolation and identification of swine influenza recombinant A/Swine/Shandong/1/2003(H9N2) virus. Microbes Infect 6(10):919–925
Yassine HM, Al-Natour MQ, Lee CW, Saif YM (2007) Interspecies and intraspecies transmission of triple reassortant H3N2 influenza A viruses. Virol J 4:129
Yassine HM, Lee CW, Suarez DL, Saif YM (2008) Genetic and antigenic relatedness of H3 subtype influenza A viruses isolated from avian and mammalian species. Vaccine 26(7):966–977
Yassine HM, Khatri M, Lee CW, Saif YM (2010) Characterization of an H3N2 triple reassortant influenza virus with a mutation at the receptor binding domain (D190A) that occurred upon virus transmission from turkeys to pigs. Virol J 7:258
Yassine HM, Khatri M, Lee CW, Saif YM (2011) Potential role of viral surface glycoproteins in the replication of H3N2 triple reassortant influenza A viruses in swine and turkeys. Vet Microbiol 148(2-4):175–182
Zhou NN, Senne DA, Landgraf JS, Swenson SL, Erickson G, Rossow K, Liu L, Yoon K, Krauss S, Webster RG (1999) Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol 73(10):8851–8856
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Yassine, H.M., Lee, CW., Saif, Y.M. (2011). Interspecies Transmission of Influenza A Viruses Between Swine and Poultry. In: Richt, J., Webby, R. (eds) Swine Influenza. Current Topics in Microbiology and Immunology, vol 370. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2011_180
Download citation
DOI: https://doi.org/10.1007/82_2011_180
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-36870-7
Online ISBN: 978-3-642-36871-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)