Swine and Influenza: A Challenge to One Health Research

Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 385)

Abstract

The challenge of increasing swine production and a rising number of novel and known swine influenza viruses has prompted a considerable boost in research into how and why pigs have become such significant hosts for influenza viruses. The ecology of influenza A viruses is rather complicated, involving multiple host species and a segmented genome. Wild aquatic birds are the reservoir for the majority of influenza A viruses, but novel influenza viruses were recently identified in bats. Occasionally, influenza A viruses can be transmitted to mammals from avian species and this event could lead to the generation of human pandemic strains. Swine are thought to be “mixing vessels” because they are susceptible to infection with both avian and mammalian influenza viruses; and novel influenza viruses can be generated in pigs by reassortment. At present, it is difficult to predict which viruses might cause a human pandemic. Therefore, both human and veterinary research needs to give more attention to the potential cross-species transmission capacity of influenza A viruses.

References

  1. Baum LG, Paulson JC (1990) Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem Suppl 40:35–38PubMedGoogle Scholar
  2. Bowman AS, Workman JD, Nolting JM, Nelson SW, Siemons RD (2014) Exploration of risk factors contributing to the presence of influenza virus in swine at agricultural fairs. Emerg Microbes Infect 3:e5CrossRefPubMedCentralGoogle Scholar
  3. Brown IH (2000) The epidemiology and evolution of influenza viruses in pigs. Vet Microbiol 74:29–46CrossRefPubMedGoogle Scholar
  4. Brown IH (2013) History and epidemiology of swine influenza in Europe. Cur Top Microbiol Immunol 370:133–146Google Scholar
  5. 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 and Thailand in 2004. J Virol 79:10821–10825CrossRefPubMedPubMedCentralGoogle Scholar
  6. Coker R, Rushton J, Mounier-Jack S, Karimuribo E, Lutumba P, Kambarage D, Pfeiffer DU, Stark K, Rweyemamu M (2011) Towards a conceptual framework to support one-health research for policy on emerging zoonoses. Lancet Infect Dis 11:326–331CrossRefPubMedGoogle Scholar
  7. 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 28:333–340PubMedGoogle Scholar
  8. Delgado C, Rosegrant M, Steinfeld H, Ehui S, Courbois C (1999) Livestock to 2020. The next food revolution. Food, agriculture and the environment. Discussion paper 28. International Food Policy Research Institute, Washington DCGoogle Scholar
  9. Ducatez MF, Hause B, Stigger-Rosser E, Darnell D, Corzo C, Juleen K, Simonson R, Brockwell-Staats C, Rubrum A, Wang D, Webb A, Crumpton JC, Lowe J, Gramer M, Webby RJ (2011) Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis 17:1624–1629CrossRefPubMedPubMedCentralGoogle Scholar
  10. Epperson S, Jhung M, Richards S, Quinlisk P, Ball L, Moll M, Boulton R, Haddy L, Biggerstaff M, Brammer L, Trock S, Burns E, Gomez T, Wong KK, Katz J, Lindstrom S, Klimov A, Bresee JS, Jernigan DB, Cox N, Finelli L (2013) Human infections with influenza A(H3N2) variant virus in the United States, 2011–2012. Clin Infect Dis 57(Suppl 1):S4–S11CrossRefPubMedGoogle Scholar
  11. Gaydos JC, Hodder RA, Top FH Jr, Allen RG, Soden VJ, Nowosiwsky T, Russell PK (1977a) Swine influenza A at Fort Dix, New Jersey (January–February 1976). II. Transmission and morbidity in units with cases. J Infect Dis 136(Suppl):S363–S368Google Scholar
  12. Gaydos JC, Hodder RA, Top FH Jr, Soden VJ, Allen RG, Bartley JD, Zabkar JH, Nowosiwsky T, Russell PK (1977b) Swine influenza A at Fort Dix, New Jersey (January–February 1976). I. Case finding and clinical study of cases. J Infect Dis 136(Suppl):S356–S362Google Scholar
  13. Gaydos JC, Top FH Jr, Hodder RA, Russell PK (2006) Swine influenza A outbreak, Fort Dix, New Jersey, 1976. Emerg Infect Dis 12:23–28CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hodder RA, Gaydos JC, Allen RG, Top FH Jr, Nowosiwsky T, Russell PK (1977) Swine influenza A at Fort Dix, New Jersey (January–February 1976). III. Extent of spread and duration of the outbreak. J Infect Dis 136(Suppl):S369–S375Google Scholar
  15. Ito T, Suzuki Y, Mitnaul L, Vines A, Kida H, Kawaoka Y (1997) Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 227:493–499CrossRefPubMedGoogle Scholar
  16. 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 72:7367–7373PubMedPubMedCentralGoogle Scholar
  17. Kageyama T, Fujisaki S, Takashita E, Xu H, Yamada S, Uchida Y, Neumann G, Saito T, Kawaoka Y, Tashiro M (2013) Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill 18:20453PubMedGoogle Scholar
  18. Keenliside J (2013) Pandemic influenza A H1N1 in Swine and other animals. Curr Top Microbiol Immunol 370:259–271PubMedGoogle Scholar
  19. Kida H, Ito T, Yasuda J, Shimizu Y, Itakura C, Shortridge KF, Kawaoka Y, Webster RG (1994) Potential for transmission of avian influenza viruses to pigs. J Gen Virol 75:2183–2188CrossRefPubMedGoogle Scholar
  20. Kimble B, Nieto GR, Perez DR (2010) Characterization of influenza virus sialic acid receptors in minor poultry species. Virol J 7:365CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kleanthous A (2009) Pigs and the environment. Here Tomorrow/BPEX, LondonGoogle Scholar
  22. Kluska V, Macku M, Mensik J (1961) Demonstration of antibodies against swine influenza viruses inman. Cesk Pediatr 16:408–414PubMedGoogle Scholar
  23. Komadina N, McVernon J, Hall R, Leder K (2014) A historical perspective of influenza A(H1N2) virus. Emerg Infect Dis 20:6–12CrossRefPubMedPubMedCentralGoogle Scholar
  24. Krauss S, Obert CA, Franks J, Walker D, Jones K, Seiler P, Niles L, Pryor SP, Obenauer JC, Naeve CW, Widjaja L, Webby RJ, Webster RG (2007) Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog 3:e167CrossRefPubMedPubMedCentralGoogle Scholar
  25. Krueger WS, Gray GC (2013) Swine influenza virus infections in man. Curr Top Microbiol Immunol 370:201–225PubMedGoogle Scholar
  26. 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:e1000102CrossRefPubMedPubMedCentralGoogle Scholar
  27. Liu W, Wei M-T, Tong Y, Tang F, Zhang L, Fang L, Yang H, Cao W-C (2011) Seroprevalence and genetic characteristics of five subtypes of influenza A viruses in the Chinese pig population: a pooled data analysis. Vet J 187:200–206CrossRefPubMedGoogle Scholar
  28. Liu Q, Ma J, Liu H, Qi W, Anderson J, Henry SC, Hesse RA, Richt JA, Ma W (2012) Emergence of novel reassortant H3N2 swine influenza viruses with the 2009 pandemic H1N1 genes in the United States. Arch Virol 157:555–562CrossRefPubMedGoogle Scholar
  29. 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, Gao GF (2013) Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381:1926–1932CrossRefPubMedGoogle Scholar
  30. Liu Q, Bin Z, Ma W, Bawa B, Ma J, Wang W, Lang Y, Lyoo Y, Halpin RA, Lin X, Stockwell TB, Webby RJ, Wentworth D, Richt JA (2014) Analysis of recombinant H7N9 wild type and mutant viruses in pigs shows Q226L in HA is important for transmission. J Virol 88(14):8153–8165 Google Scholar
  31. Lymbery P, Oakeshott I (2014) Farmageddon: the true cost of cheap meat. Bloomsbury, LondonGoogle Scholar
  32. 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 USA 104:20949–20954CrossRefPubMedPubMedCentralGoogle Scholar
  33. Ma W, Kahn RE, Richt JA (2009) The pig as a mixing vessel for influenza viruses: human and veterinary implications. J Mol Genet Med 3:158–166CrossRefPubMedCentralGoogle Scholar
  34. Marks JS, Halpin TJ (1980) Guillain-Barre syndrome in recipients of A/New Jersey influenza vaccine. JAMA 243:2490–2494CrossRefPubMedGoogle Scholar
  35. Milinovich GJ, Williams GM, Clements ACA, Hu W (2014) Internet-based surveillance systems for monitoring emerging infectious diseases. Lancet Infect Dis 14:160–168CrossRefPubMedGoogle Scholar
  36. Morens DM, Taubenberger JK (2014) A possible outbreak of swine influenza, 1892. Lancet Infect Dis 14:169–172CrossRefPubMedGoogle Scholar
  37. Myers KP, Olsen CW, Gray GC (2007) Cases of swine influenza in humans: a review of the literature. Clin Infect Dis 44:1084–1088CrossRefPubMedPubMedCentralGoogle Scholar
  38. National Bureau of Statistics of China (2014) China’s economy showed good momentum of steady growth in the year of 2013. www.stats.gov.cn/english/pressrelease/201401/tp140120_502079.html
  39. Neustadt RE, Fineberg HV (1978/2005) The swine flu affair: decision-making on a slippery disease. University Press of the Pacific, HonoluluGoogle Scholar
  40. Osterholm MT, Kelley NS, Sommer A, Belongia EA (2012) Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 12:36–44CrossRefPubMedGoogle Scholar
  41. Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL, Lai RW, Orr WK, Shortridge KF (1999) Human infection with influenza H9N2. Lancet 354:916–917CrossRefPubMedGoogle Scholar
  42. 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 75:9679–9686CrossRefPubMedPubMedCentralGoogle Scholar
  43. Qiao C, Liu Q, Bawa B, Shen H, Qi W, Chen Y, Mok CK, Garcia-Sastre A, Richt JA, Ma W (2012) Pathogenicity and transmissibility of reassortant H9 influenza viruses with genes from pandemic H1N1 virus. J Gen Virol 93:2337–2345CrossRefPubMedPubMedCentralGoogle Scholar
  44. Richt JA, Webby R (eds) (2013) Swine influenza. Curr Top Microbiol Immunol 370:1–300 Google Scholar
  45. Richt JA, Webby R, Kahn RE (2013) The pandemic H1N1 influenza experience. In: Mackenzie JS, Jeggo M, Daszak PS, Richt JA (eds) One health: the human–animal-environment interfaces in emerging infectious disease: the concept and examples of a one health approach. Current topics in microbiology and immunology, vol 365, pp 269–280Google Scholar
  46. Rogers GN, D’Souza BL (1989) Receptor binding properties of human and animal H1 influenza virus isolates. Virology 173:317–322CrossRefPubMedGoogle Scholar
  47. Rogers GN, Paulson JC (1983) Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127:361–373CrossRefPubMedGoogle Scholar
  48. Scholtissek C, Burger H, Kistner O, Shortridge KF (1985) The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 147:287–294CrossRefPubMedGoogle Scholar
  49. Schrauwen EJA, Fouchier RAM (2014) Host adaptation and transmission of influenza A viruses in mammals. Emerg Microbes Infect 3:e9CrossRefPubMedCentralGoogle Scholar
  50. Sencer DJ, Millar JD (2006) Reflections on the 1976 swine flu vaccination program. Emerg Infect Dis 12:29–33CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y (2006) Avian flu: influenza virus receptors in the human airway. Nature 440:435–436CrossRefPubMedGoogle Scholar
  52. Silverstein AM (1981) Pure politics and impure science: the swine flu affair. Johns Hopkins University Press, BaltimoreGoogle Scholar
  53. Simonsen L, Spreeuwenberg P, Lustig R, Taylor RJ, Fleming DM, Kroneman M, Van Kerkhove MD, Mounts AW, Paget WJ (2013) Global mortality estimates for the 2009 influenza pandemic from the GLaMOR project: a modeling study. PLoS Med 10:e1001558CrossRefPubMedPubMedCentralGoogle Scholar
  54. Smith TF, Burgert EO Jr, Dowdle WR, Noble GR, Campbell RJ, Van Scoy RE (1976) Isolation of swine influenza virus from autopsy lung tissue of man. N Engl J Med 294:708–710CrossRefPubMedGoogle Scholar
  55. Suzuki Y (2005) Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol Pharm Bull 28:399–408CrossRefPubMedGoogle Scholar
  56. Suzuki T, Horiike G, Yamazaki Y, Kawabe K, Masuda H, Miyamoto D, Matsuda M, Nishimura SI, Yamagata T, Ito T, Kida H, Kawaoka Y, Suzuki Y (1997) Swine influenza virus strains recognize sialylsugar chains containing the molecular species of sialic acid predominantly present in the swine tracheal epithelium. FEBS Lett 404:192–196CrossRefPubMedGoogle Scholar
  57. Suzuki Y, Ito T, Suzuki T, Holland RE Jr, Chambers TM, Kiso M, Ishida H, Kawaoka Y (2000) Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 74:11825–11831CrossRefPubMedPubMedCentralGoogle Scholar
  58. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, Xu X, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO (2012) A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci USA 109:4269–4274CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9:e1003657CrossRefPubMedPubMedCentralGoogle Scholar
  60. Top FH Jr, Russell PK (1977) Swine influenza A at Fort Dix, New Jersey (January–February 1976). IV. Summary and speculation. J Infect Dis 136(Suppl):S376–S380Google Scholar
  61. Vincent AL, Ma W, Lager KM, Janke BH, Richt JA (2008) Swine influenza viruses a North American perspective. Adv Virus Res 72:127–154CrossRefPubMedGoogle Scholar
  62. Vincent A, Awada L, Brown I, Chen H, Claes F, Dauphin G, Donis R, Culhane M, Hamilton K, Lewis N, Mumford E, Nguyen T, Parchariyanon S, Pasick J, Pavade G, Pereda A, Peiris F (2014) Review of influenza A virus in swine worldwide: a call for increased surveillance and research. Zoonoses Public Health 61:4–17Google Scholar
  63. Wan H, Perez DR (2006) Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 346:278–286CrossRefPubMedGoogle Scholar
  64. Weis T (2013) The ecological hoofprint: the global burden of industrial livestock. Zed Books, LondonGoogle Scholar
  65. Worldometers (2014) World population. www.worldometers.info/world-population/
  66. Wu Y, Tefsen B, Shi Y, Gao GF (2014) Bat-derived influenza-like viruses H17N10 and H18N11. Trends Microbiol 22:183–191CrossRefPubMedGoogle Scholar
  67. Yassine HM, Al-Natour MQ, Lee CW, Saif YM (2007) Interspecies and intraspecies transmission of triple reassortant H3N2 influenza A viruses. Virol J 4:129CrossRefPubMedPubMedCentralGoogle Scholar
  68. Zhang G, Kong W, Qi W, Long LP, Cao Z, Huang L, Qi H, Cao N, Wang W, Zhao F, Ning Z, Liao M, Wan XF (2011) Identification of an H6N6 swine influenza virus in southern China. Infect Genet Evol 11:1174–1177CrossRefPubMedPubMedCentralGoogle Scholar
  69. Zhao G, Chen C, Huang J, Wang Y, Peng D, Liu X (2013) Characterisation of one H6N6 influenza virus isolated from swine in China. Res Vet Sci 95:434–436CrossRefPubMedGoogle Scholar
  70. 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 73:8851–8856PubMedPubMedCentralGoogle Scholar
  71. Zhu H, Webby R, Lam TT, Smith DK, Peiris JS, Guan Y (2013) History of swine influenza viruses in Asia. Curr Top Microbiol Imunol 370:57–68Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.College of Veterinary Medicine, Diagnostic Medicine/PathobiologyKansas State UniversityManhattanUSA

Personalised recommendations