Archives of Virology

, Volume 163, Issue 2, pp 359–364 | Cite as

Evidence of infection with avian, human, and swine influenza viruses in pigs in Cairo, Egypt

  • Mokhtar R. Gomaa
  • Ahmed Kandeil
  • Rabeh El-Shesheny
  • Mahmoud M. Shehata
  • Pamela P. McKenzie
  • Richard J. Webby
  • Mohamed A. Ali
  • Ghazi Kayali
Original Article


The majority of the Egyptian swine population was culled in the aftermath of the 2009 H1N1 pandemic, but small-scale growing remains. We sampled pigs from piggeries and an abattoir in Cairo. We found virological evidence of infection with avian H9N2 and H5N1 viruses as well as human pandemic H1N1 influenza virus. Serological evidence suggested previous exposure to avian H5N1 and H9N2, human pandemic H1N1, and swine avian-like and human-like viruses. This raises concern about potential reassortment of influenza viruses in pigs and highlights the need for better control and prevention of influenza virus infection in pigs.



This work was funded by the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under contract number HHSN272201400006C, and supported by the American Lebanese Syrian Associated Charities (ALSAC).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


This study was funded by the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under contract number HHSN272201400006C, and supported by the American Lebanese Syrian Associated Charities (ALSAC).

Ethical approval

All applicable international, national, and/or institutional guidelines for the care of animals were followed. This article does not contain any studies with human participants performed by any of the authors.


  1. 1.
    Abdelwhab EM, Abdel-Moneim AS (2015) Epidemiology, ecology and gene pool of influenza A virus in Egypt: will Egypt be the epicentre of the next influenza pandemic? Virulence 6:6–18CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    El-Sayed A, Awad W, Fayed A, Hamann HP, Zschock M (2010) Avian influenza prevalence in pigs, Egypt. Emerg Infect Dis 16:726–727CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    El-Shesheny R, Kandeil A, Bagato O, Maatouq AM, Moatasim Y, Rubrum A, Song MS, Webby RJ, Ali MA, Kayali G (2014) Molecular characterization of avian influenza H5N1 virus in Egypt and the emergence of a novel endemic subclade. J Gen Virol 95:1444–1463CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Fuller TL, Gilbert M, Martin V, Cappelle J, Hosseini P, Njabo KY, Aziz SA, Xiao X, Daszak P, Smith TB (2013) Predicting hotspots for influenza virus reassortment. Emerg Infect Dis 19:581–588CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, Fouchier RA, Pappas C, Alpuche-Aranda CM, Lopez-Gatell H, Olivera H, Lopez I, Myers CA, Faix D, Blair PJ, Yu C, Keene KM, Dotson PD Jr, Boxrud D, Sambol AR, Abid SH, St George K, Bannerman T, Moore AL, Stringer DJ, Blevins P, Demmler-Harrison GJ, Ginsberg M, Kriner P, Waterman S, Smole S, Guevara HF, Belongia EA, Clark PA, Beatrice ST, Donis R, Katz J, Finelli L, Bridges CB, Shaw M, Jernigan DB, Uyeki TM, Smith DJ, Klimov AI, Cox NJ (2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146:2275–2289CrossRefPubMedGoogle Scholar
  7. 7.
    Kandeil A, El-Shesheny R, Maatouq AM, Moatasim Y, Shehata MM, Bagato O, Rubrum A, Shanmuganatham K, Webby RJ, Ali MA, Kayali G (2014) Genetic and antigenic evolution of H9N2 avian influenza viruses circulating in Egypt between 2011 and 2013. Arch Virol 159:2861–2876CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Kayali G, Kandeil A, El-Shesheny R, Kayed AS, Gomaa MM, Maatouq AM, Shehata MM, Moatasim Y, Bagato O, Cai Z, Rubrum A, Kutkat MA, McKenzie PP, Webster RG, Webby RJ, Ali MA (2014) Active surveillance for avian influenza virus, Egypt, 2010–2012. Emerg Infect Dis 20:542–551CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Lee MS, Chang PC, Shien JH, Cheng MC, Shieh HK (2001) Identification and subtyping of avian influenza viruses by reverse transcription-PCR. J Virol Methods 97:13–22CrossRefPubMedGoogle Scholar
  10. 10.
    Ma W, Kahn RE, Richt JA (2008) The pig as a mixing vessel for influenza viruses: human and veterinary implications. J Mol Genet Med 3:158–166PubMedPubMedCentralGoogle Scholar
  11. 11.
    Meseko C, Olaleye D, Capua I, Cattoli G (2014) Swine influenza in sub-saharan Africa–current knowledge and emerging insights. Zoonoses Public Health 61:229–237CrossRefPubMedGoogle Scholar
  12. 12.
    Nelson MI, Vincent AL (2015) Reverse zoonosis of influenza to swine: new perspectives on the human-animal interface. Trends Microbiol 23:142–153CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Seef S, Jeppsson A (2013) Is it a policy crisis or it is a health crisis? The Egyptian context-analysis of the Egyptian health policy for the H1N1 flu pandemic control. Pan Afr Med J 14:59PubMedPubMedCentralGoogle Scholar
  14. 14.
    Shalaby MA, Nafi BM, Saber MS, Hosny AH (1981) Serological studies on swine influenza in Egypt. Int J Zoonoses 8:100–106PubMedGoogle Scholar
  15. 15.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    WHO (2002) WHO manual on animal influenza diagnosis and surveillance. WHO, Geneva.
  17. 17.
    WHO (2010) Serological diagnosis of influenza by microneutralization assayGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria 2017

Authors and Affiliations

  1. 1.Center of Scientific Excellence for Influenza Viruses, National Research CenterGizaEgypt
  2. 2.Department of Infectious DiseasesSt. Jude Children’s Research HospitalMemphisUSA
  3. 3.Department of Epidemiology, Human Genetics, and Environmental SciencesUniversity of Texas Health Sciences CenterHoustonUSA
  4. 4.Human LinkBaabdaLebanon

Personalised recommendations