Pig lung immune cytokine response to the swine influenza virus and the Actinobacillus pleuropneumoniae infection


Introduction: The aim of this study was to evaluate and compare the local innate immune response to the swine influenza virus (SIV) and Actinobacillus pleuropneumoniae (App) infection in pigs. Material and Methods: The study was performed on 37 seven-week-old pigs, divided into four groups: App-infected (n=11), App+SIV-infected (n=11), SIV-infected (n=11), and control (n=4). Lung samples were collected, following euthanasia, on the 2nd and 4th dpi (three piglets per inoculated group) and on the 10th dpi (remaining inoculated and control pigs). Lung concentrations of IL-1β, IL-6, IL-8, TNF-α, IL-10, IFN-α, and IFN-γ were analysed with the use of commercial porcine cytokine ELISA kits. Results: Lung concentrations of IL-1β, IL-6, IL-8, TNF-α, IFN-α, and IFN-γ were induced in SIV-infected and App+SIV-infected pigs. In the lung tissue of App-infected pigs, only concentrations of IL-1β, IL-6, IL-8, and IFN-γ were elevated. Additionally, in App+SIV-infected pigs, significantly greater concentrations of IL-1β, IL-8, and IFN-α were found when compared with pigs infected with either SIV or App alone. In each tested group, the lung concentration of IL-10 remained unchanged during the entire study. Conclusion: The results of the study indicate that the experimental infection of pigs with SIV or App alone and co-infection with both pathogens induced a local lung inflammatory response. However, the local cytokine response was considerably higher in co-infected pigs compared to singleinfected pigs

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • 1. Baarsch M.J., Scamurra R.W., Burger K., Foss D.L., Maheswaran S.K., Murtaugh M.P.: Inflammatory cytokine expression in swine experimentally infected with Actinobacillus pleuropneumoniae. Infect Immun 1995, 63, 3587-3594.

  • 2. Balaji R., Wright K.J., Turner J.L., Hill C.M., Dritz S.S., Fenwick B., Carroll J.A., Zannelli M.E., Beasang L.A., Minton J.E.: Circulating cortisol, tumor necrosis factor-α, interleukin-1β, and interferon-γ in pigs infected with Actinobacillus pleuropneumoniae. J Anim Sci 2002, 80, 202-207.

  • 3. Barbé F., Saelens X., Braeckmans D., Lefèvre F., van Reeth K.: Role of IFN-alpha during the acute stage of a swine influenza virus infection. Res Vet Sci 2010, 88, 172-178.

  • 4. Barbé F., Atanasova K., Van Reeth K.: Cytokines and acute phase proteins associated with acute swine influenza infection in pigs. Vet J 2011, 187, 48-53.

  • 5. Benga L., Hoeltig D., Rehm T., Rothkoetter H.J., Pabst R., Valentin-Weigand P., FUGATO-consortium IRAS. Expression levels of immune markers in Actinobacillus pleuropneumoniae infected pigs and their relation to breed and clinical symptoms. BMC Vet Res 2009, 5, 13.

  • 6. Bossé J.T., Janson H., Sheehan B.J., Beddek A.J., Rycroft A.N., Kroll J.S., Langford P.R.: Actinobacillus pleuropneumoniae: pathobiology and pathogenesis of infection. Microb Infect 2002, 4, 225-235.

  • 7. Bossé J.T., Li Y., Sárközi R., Gottschalk M., Angen Ø., Nedbalcova K., Rycroft A.N., Fodor L., Langford P.R.: A unique capsule locus in the newly designated Actinobacillus pleuropneumoniae serovar 16 and development of a diagnostic PCR. J Clin Microbiol 2017, 55, 902-907.

  • 8. Brauer C., Hennig-Pauka I., Hoeltig D., Buettner F.F., Beyerbach M., Gasse H., Gerlach G.F., Waldmann K.H.: Experimental Actinobacillus pleuropneumoniae challenge in swine: comparison of computed tomographic and radiographic findings during disease. BMC Vet Res 2012, 8, 47.

  • 9. Chen Z.W., Chien M.S., Chang N.Y., Chen T.H., Wu C.M., Huang C., Lee W.C., Hsuan S.L.: Mechanisms underlying Actinobacillus pleuropneumoniae exotoxin ApxI induced expression of IL-1β, IL-8, and TNF-α in porcine alveolar macrophages. Vet Res 2011, 42, 25.

  • 10. Chiers K., De Waele T., Pasmans F., Ducatelle R., Haesebrouck F.: Virulence factors of Actinobacillus pleuropneumoniae involved in colonization, persistence and induction of lesions in its porcine host. Vet Res 2010, 41, 65.

  • 11. Damjanovic D., Divangahi M., Kugathasan K., Small C.L., Zganiacz A., Brown E.G., Hogaboam C.M., Gauldie J., Xing Z.: Negative regulation of lung inflammation and immunopathology by TNF-α during acute influenza infection. Am J Pathol 2011, 179, 2963-2976.

  • 12. Davidson S., Crotta S., McCabe T.M., Wack A.: Pathogenic potential of interferon αβ in acute influenza infection. Nat Commun 2014, 5, 3864.

  • 13. Fossum C., Wattrang E., Fuxler L., Jensen K.T., Wallgren P.: Evaluation of various cytokines (IL-6, IFN-alpha, IFN-gamma, TNF-alpha) as markers for acute bacterial infection in swine-a possible role for serum interleukin-6. Vet Immunol Immunopathol 1998, 64, 161-172.

  • 14. Gottschalk M., Lacouture S.: Actinobacillus pleuropneumoniae serotypes 3, 6, 8, and 15 isolated from diseased pigs in North America. Vet Rec 2014, 174, 452.

  • 15. Jabłoński A., Popławski R., Jędryczko R., Pomorska-Mól M., Pejsak Z.: Prevalence of Actinobacillus pleuropneumoniae serovars in Poland. Abstracts Book of 24th International Pig Veterinary Society Congress, Dublin, Ireland, 2016, p. 175.

  • 16. Jonasch E., Haluska F.G.: Interferon in oncological practice: review of interferon biology, clinical applications, and toxicities. Oncologist 2001, 6, 34-55.

  • 17. Kowalczyk A., Pomorska-Mól M., Kwit K., Pejsak Z., Rachubik J., Markowska-Daniel I.: Cytokine and chemokine mRNA expression profiles in BALF cells isolated from pigs single infected or co-infected with swine influenza virus and Bordetella bronchiseptica. Vet Microbiol 2014, 170, 206-112.

  • 18. Lauder S.N., Jones E., Smart K., Bloom A., Williams A.S., Hindley J.P., Ondondo B., Taylor P.R., Clement M., Fielding C., Godkin A.J., Jones S.A., Gallimore A.M.: Interleukin-6 limits influenza-induced inflammation and protects against fatal lung pathology. Eur J Immunol 2013, 43, 2613-2625.

  • 19. Levesque C., Provost C., Labrie J., Hernandez Reyes Y., Burciaga Nava J.A., Gagnon C.A., Jacques M.: Actinobacillus pleuropneumoniae possesses an antiviral activity against porcine reproductive and respiratory syndrome virus. PLoS One 9, 2014, e98434.

  • 20. Loving C.L., Brockmeier S.L., Vincent A.L., Palmer M.V., Sacco R.E., Nicholson T.L.: Influenza virus coinfection with Bordetella bronchiseptica enhances bacterial colonization and host responses exacerbating pulmonary lesions. Microb Pathog 2010, 49, 237-245.

  • 21. Madec F., Kobisch M.: Bilan lésionnel des porcs charcutiers à l’abattoir. J Rech Porc Fr 1982, 1414, 405-412.

  • 22. Opriessnig T., Gimenez-Lirola L.G., Halbur P.G.: Polymicrobial respiratory disease in pigs. Anim Health Res Rev 2011, 12, 133-148.

  • 23. Pomorska-Mól M., Markowska-Daniel I., Kwit K., Stępniewska K., Pejsak Z.: C-reactive protein, haptoglobin, serum amyloid A and pig major acute phase protein response in pigs simultaneously infected with H1N1 swine influenza virus and Pasteurella multocida. BMC Vet Res 2013, 9, 14.

  • 24. Pomorska-Mól M., Kwit K., Markowska-Daniel I., Kowalski C., Pejsak Z.: Local and systemic immune response in pigs during subclinical and clinical swine influenza infection. Res Vet Sci 2014, 97, 412-421.

  • 25. Pomorska-Mól M., Markowska-Daniel I., Kwit K., Czyżewska E., Dors A., Rachubik J., Pejsak Z.: Immune and inflammatory response in pigs during acute influenza caused by H1N1 swine influenza virus. Arch Virol 2014, 159, 2605-2614.

  • 26. Pomorska-Mól M., Dors A., Kwit K., Kowalczyk A., Stasiak E., Pejsak Z.: Kinetics of single and dual infection of pigs with swine influenza virus and Actinobacillus pleuropneumoniae. Vet Microbiol 2017, 201, 113-120.

  • 27. Sibila M., Aragon V., Fraile L., Segales J.: Comparison of four lung scoring systems for the assessment of the pathological outcomes derived from Actinobacillus pleuropneumoniae experimental infections. BMC Vet Res 2014, 10, 165.

  • 28. van Gucht S., Labarque G., van Reeth K.: The combination of PRRS virus and bacterial endotoxin as a model for multifactorial respiratory disease in pigs. Vet Immunol Immunopathol 2004, 102, 165-178.

  • 29. van Reeth K., Nauwynck H.: Proinflammatory cytokines and viral respiratory disease in pigs. Vet Res 2000, 31, 187-213.

  • 30. van Reeth K., van Gucht S., Pensaert M.: Correlations between lung proinflammatory cytokine levels, virus replication, and disease after swine influenza virus challenge of vaccinationimmune pigs. Viral Immunol 2002, 15, 583-594.

  • 31. Wang L., Qin W., Zhang J., Bao C., Zhang H., Che Y., Sun C., Gu J., Feng X., Du C., Han W., Richard P.L., Lei L.: Adh enhances Actinobacillus pleuropneumoniae pathogenicity by binding to OR5M11 and activating p38 which induces apoptosis of PAMs and IL-8 release. Sci Rep 2016, 6, 24058.


Journal + Issues