Vet Med - Czech, 2013, 58(4):206-220 | DOI: 10.17221/6759-VETMED

The respiratory tract in pigs and its immune system: a reviewReview

J. Krejci, K. Nechvatalova, M. Blahutkova, M. Faldyna
Veterinary Research Institute, Brno, Czech Republic

The growing amount of information regarding mucosal immunology in animals resulted from a need to better understand the pathogenesis of diseases entering the body through mucosa surfaces, including the respiratory tract. The second reason for such studies is associated with a search for alternative ways of vaccine application, including delivery to the mucosa of the respiratory tract. This review provides a structural and functional description of the immune system of the pig respiratory tract.

Keywords: swine; histology; host defence; specific immunity; innate immunity

Published: April 30, 2013  Show citation

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Krejci J, Nechvatalova K, Blahutkova M, Faldyna M. The respiratory tract in pigs and its immune system: a review. Vet Med-Czech. 2013;58(4):206-220. doi: 10.17221/6759-VETMED.
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References

  1. Adlerova L, Bartoskova A, Faldyna M (2008): Lactoferrin: a review. Veterinarni Medicina 53, 457-468. Go to original source...
  2. Bailey M, Stokes CR (1998): Mucosal immunity. In: Pastoret PP, Griebel P, Bazin H, Govaerts A (eds.): Handbook of Vertebrate Immunology. 1st ed. Academic Press, San Diego. 402-405.
  3. Bartlett JA, Fischer AJ, McCray PB Jr. (2008): Innate immune functions of the airway epithelium. Contributor to Microbiology 15, 147-163. Go to original source... Go to PubMed...
  4. Baskerville A (1970a): Ultrastructural studies of the normal pulmonary tissue of the pig. Research in Veterinary Sciences, 11, 150-155. Go to original source...
  5. Baskerville A (1970b): Ultrastructure of the bronchial epithelium of the pig. Zentralblatt Veterinärmedizin Reihe A 17, 796-802. Go to original source... Go to PubMed...
  6. Bertram TA (1986): Intravascular macrophages in lungs of pigs infected with Haemophilus pleuropneumoniae. Veterinary Pathology 23, 681-691. Go to original source... Go to PubMed...
  7. Bienenstock J, Clancy RL (1994): Bronchial mucosal lymphoid tissue. In: Ogra PL, Strober W (eds.): Handbook of Mucosal Immunology. 1st ed. Academic Press, San Diego. 529-538. Go to original source...
  8. Bienenstock J, Rudzik O, Clancy RL, Perey DY (1974): Bronchial lymphoid tissue. Advances in Experimental Medicine and Biology 45, 47-56. Go to original source... Go to PubMed...
  9. Bienenstock J., McDermott M.R., Clancy R.L. (1999): Respiratory tract defenses: Role of mucosal lymphoid tissues. In: Ogra PL, Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR (eds.), Mucosal Immunology. 2nd ed. Academic Press, San Diego. 283-292.
  10. Binns RM, Pabst R (1994): Lymphoid tissue structure and lymphocyte trafficking in the pig. Veterinary Immunology and Immunopathology 43, 79-87. Go to original source... Go to PubMed...
  11. Bourges D, Chevaleyre C, Wang C, Berri M, Zhang X, Nicaise L, Meurens F, Salmon H (2007): Differential expression of adhesion molecules and chemokines between nasal and small intestinal mucosae: implications for T- and sIgA+ B-lymphocyte recruitment. Immunology 122, 551-561. Go to original source... Go to PubMed...
  12. Bradley PA, Bourne FJ, Brown PJ (1976a): The respiratory tract immune system in the pigs. I. Distribution of immunoglobulin-containing cells in the respiratory tract mucosa. Veterinary Pathology 13, 81-89. Go to original source... Go to PubMed...
  13. Bradley PA, Bourne FJ, Brown PJ (1976b): The respiratory tract immune system in the pigs. II. Associated lymphoid tissue. Veterinary Pathology 13, 90-97. Go to original source... Go to PubMed...
  14. Brandtzaeg P, Farstad IN, Haraldsen G (1999): Regional specialization in the mucosal immune system: primed cells do not always home along the same tract. Immunology Today 20, 267-277. Go to original source... Go to PubMed...
  15. Breeze RG, Wheeldon EB, Pirie HM (1976): Cell structure and function in the mammalian lung: the trachea, bronchi and bronchioles. Veterinary Bulletin 46, 319-337.
  16. Charley B, Corthier G (1977): Local immunity in the respiratory tract. II. Relationship of serum and local antibodies. Annales de Microbiologie 128B, 109-119. Go to PubMed...
  17. Chitko-McKown CG, Blecha F (1992): Pulmonary intravascular macrophages: a review of immune properties and functions. Annales de Recherches Veterinaires 23, 201-214. Go to PubMed...
  18. Cone R.A. (1999): Mucus. In: Ogra PL, Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR (eds.): Mucosal Immunology. 2nd ed. Academic Press, San Diego. 43-64.
  19. Crocker SH, Lowery BD, Eddy DO, Wismar BL, Buesching WJ, Obenauf RN (1981): Pulmonary clearance of blood-borne bacteria. Surgery Gynecology and Obsterics 153, 845-851.
  20. Crouch EC (1998): Collectins and pulmonary host defense. American Journal of Respiratory Cell and Molecular Biology 19, 177-201. Go to original source... Go to PubMed...
  21. Cruijsen TL, van Leengoed LA, Dekker-Nooren TC, Schoevers EJ, Verheijden JH (1992): Phagocytosis and killing of Actinobacillus pleuropneumoniae by alveolar macrophages and polymorphonuclear leukocytes isolated from pigs. Infection and Immunity 60, 4867-4871. Go to original source... Go to PubMed...
  22. DeBey MC, Ross RF (1994): Ciliostasis and loss of cilia induced by Mycoplasma hyopneumoniae in porcine tracheal organ cultures. Infection and Immunity 62, 5312-5318. Go to original source... Go to PubMed...
  23. DeBey MC, Jacobson CD, Ross RF (1992): Histochemical and morphologic changes of porcine airway epithelial cells in response to infection with Mycoplasma hyopneumoniae. American Journal of Veterinary Research 53, 1705-1710.
  24. Delventhal S, Brandis A, Ostertag H, Pabst R (1992): Low incidence of bronchus-associated lymphoid tissue (BALT) in chronically inflamed human lungs. Virchows Archiv B: Cell Pathology 62, 271-274. Go to original source... Go to PubMed...
  25. Dunkley M, Pabst R, Cripps A (1995): An important role for intestinally derived T cells in respiratory defense. Immunology Today 16, 231-236. Go to original source... Go to PubMed...
  26. Erle DJ, Pabst R (2000): Intraepithelial lymphocytes in the lung: a neglected lymphocyte population. American Journal of Respiratory Cell and Molecular Biology 22, 398-400. Go to original source... Go to PubMed...
  27. Euzeby JP (1993): The immune system of the respiratory tract of the pig: A review (In French). Revue de Medicine Veterinaire 144, 665-681.
  28. Faldyna M, Nechvatalova K, Sinkora J, Knotigova P, Leva L, Krejci J, Toman M (2005): Experimental Actinobacillus pleuropneumoniae infection in piglets with different types and levels of specific protection: immunophenotypic analysis of lymphocyte subsets in the circulation and respiratory mucosal lymphoid tissue. Veterinary Immunology and Immunopathology 107, 143-152. Go to original source... Go to PubMed...
  29. Fournier M, Lebargy F, Le Roy Ladurie F, Lenormand E, Pariente R (1989): Intraepithelial T-lymphocyte subsets in the airways of normal subjects and of patients with chronic bronchitis. American Review of Respiratory Disease 140, 737-742. Go to original source... Go to PubMed...
  30. Ganz T (1999): Defensins and host defense. Science 286, 420-421. Go to original source... Go to PubMed...
  31. Gomez MI, Prince A (2008): Airway epithelial cell signaling in response to bacterial pathogens. Pediatric Pulmonology 43, 11-19. Go to original source... Go to PubMed...
  32. Gon Y (2008): Toll-like receptors and airway inflammation. Allergology International 57, 33-37. Go to original source... Go to PubMed...
  33. Goto E, Kohrogi H, Hirata N, Tsumori K, Hirosako S, Hamamoto J, Fuji K, Kawano O, Ando M (2000): Human bronchial intraepithelial T lymphocytes as a distinct T-cell subset: their long-term survival in SCID-Hu chimeras. American Journal of Respiratory Cell and Molecular Biology 22, 405-411. Go to original source... Go to PubMed...
  34. Haagsman HP, Hogenkamp A, van Eijk M, Veldhuizen EJ (2008): Surfactant collectins and innate immunity. Neonatology 93, 288-294. Go to original source... Go to PubMed...
  35. Hameleers DM, Stoop AE, van der Ven I, Biewenga J, van der Baan S, Sminia T (1989): Intra-epithelial lymphocytes and non-lymphoid cells in the human nasal mucosa. International Archives of Allergy and Applied Immunology 88, 317-322. Go to original source... Go to PubMed...
  36. Havenith CE, van Miert PP, Breedijk AJ, Beelen RH, Hoefsmit EC (1993): Migration of dendritic cells into the draining lymph nodes of the lung after intratracheal instillation. American Journal of Respiratory Cell and Molecular Biology 9, 484-488. Go to original source... Go to PubMed...
  37. Hermans C, Bernard A (1998): Pneumoproteinaemia: a new perspective in the assessment of lung disorders. European Respiratory Journal 11, 801-803. Go to original source... Go to PubMed...
  38. Hiemstra PS (2007): The role of epithelial beta-defensins and cathelicidins in host defense of the lung. Experimental Lung Research 33, 537-542. Go to original source... Go to PubMed...
  39. Hingley ST, Hastie AT, Kueppers F, Higgins ML (1986): Disruption of respiratory cilia by proteases including those of Pseudomonas aeruginosa. Infection and Immunity 54, 379-385. Go to original source... Go to PubMed...
  40. Hoek RM, Ruuls SR, Murphy CA, Wright GJ, Goddard R, Zurawski SM, Blom B, Homola ME, Streit WJ, Brown MH, Barclay AN, Sedgwick JD (2000): Downregulation of the macrophage lineage through interaction with OX2 (CD200). Science 290, 1768-1771. Go to original source... Go to PubMed...
  41. Holmgren N (1973): Immunoglobulins in normal porcine tracheobronchial secretions. Acta Veterinaria Scandinavica 14, 366-380. Go to original source... Go to PubMed...
  42. Holt PG (2000): Antigen presentation in the lung. American Journal of Respiratory and Critical Care Medicine 162, 151-156. Go to original source... Go to PubMed...
  43. Holt PG, Leivers S (1982): Tolerance induction via antigen inhalation: isotype specificity, stability, and involvement of suppressor T cells. International Archives of Allergy and Applied Immunology 67, 155-160. Go to original source... Go to PubMed...
  44. Holt PG, Robinson BW, Reid M, Kees UR, Warton A, Dawson VH, Rose A, Schon-Hegrad M, Papadimitriou JM (1986): Extraction of immune and inflammatory cells from human lung parenchyma: evaluation of an enzymatic digestion procedure. Clinical and Experimental Immunology 66, 188-200. Go to PubMed...
  45. Holt PG, Schon-Hegrad MA, Phillips MJ, McMenamin PG (1989): Ia-positive dendritic cells form a tightly meshed network within the human airway epithelium. Clinical and Experimental Allergy 19, 597-601. Go to original source... Go to PubMed...
  46. Holt PG, Schon-Hegrad MA, McMenamin PG (1990): Dendritic cells in the respiratory tract. International Review in Immunology 6, 139-149. Go to original source... Go to PubMed...
  47. Huang YT, Chu RM, Liu RS, Weng CN (1990): Morphologic studies of intrapulmonary airway mucosa-associated lymphoid tissues in swine. Veterinar y Immunology and Immunopathology 25, 13-22. Go to original source... Go to PubMed...
  48. Jericho KW (1970): Intrapulmonary lymphoid tissue of healthy pigs. Research in Veterinary Sciences 11, 548- 552. Go to original source...
  49. Jiang-Shieh YF, Chien HF, Chang CY, Wei TS, Chiu MM, Chen HM, Wu CH (2010): Distribution and expression of CD200 in the rat respiratory system under normal and endotoxin-induced pathological conditions. Journal of Anatomy 216, 407-416. Go to original source... Go to PubMed...
  50. Kamp EM, Kimman TG (1988): Induction of nasal turbinate atrophy in germ-free pigs, using Pasteurella multocida as well as bacterium-free crude and purified dermonecrotic toxin of P. multocida. American Journal of Veterinary Research 49, 1844-1849.
  51. Kato A, Schleimer RP (2007): Beyond inflammation: airway epithelial cells are at the interface of innate and adaptive immunity. Current Opinion in Immunology 19, 711-720. Go to original source... Go to PubMed...
  52. Krejci J, Nechvatalova K, Kudlackova H, Faldyna M, Kucerova Z, Toman M (2005): Systemic and local antibody responses after experimental infection with Actinobacillus pleuropneumoniae in piglets with passive or active immunity. Journal of Veterinary Medicine B: Infectious Diseases and Veterinary Public Health 52, 190-196. Go to original source... Go to PubMed...
  53. Kuper CF, Koornstra PJ, Hameleers DM, Biewenga J, Spit BJ, Duijvestijn AM, van Breda Vriesman PJ, Sminia T (1992): The role of nasopharyngeal lymphoid tissue. Immunology Today 13, 219-224. Go to original source... Go to PubMed...
  54. Kuper CF, Arts JH, Feron VJ (2003): Toxicity to nasalassociated lymphoid tissue. Toxicology Letters 140- 141, 281-285. Go to original source... Go to PubMed...
  55. Liebler-Tenorio EM, Pabst R (2006): MALT structure and function in farm animals. Veterinary Research 37, 257-280. Go to original source... Go to PubMed...
  56. Mair TS, Batten EH, Stokes CR, Bourne FJ (1987): The histological features of the immune system of the equine respiratory tract. Journal of Comparative Pathology 97, 575-586. Go to original source... Go to PubMed...
  57. Marriott HM, Dockrell DH (2007): The role of the macrophage in lung disease mediated by bacteria. Experimental Lung Research 33, 493-505. Go to original source... Go to PubMed...
  58. McDermott MR, Bienenstock J (1979): Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. Journal of Immunology 122, 1892-1898. Go to original source... Go to PubMed...
  59. McWilliam AS, Nelson D, Thomas JA, Holt PG (1994): Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces. Journal of Experimental Medicine 179, 1331-1336. Go to original source... Go to PubMed...
  60. Mensik J, Franz J, Pospisil Z, Krejci J (1971a): The local transport of antibodies in the protection of calves and piglets against viral respiratory infection. Acta Veterinaria Brno 2, 75-81.
  61. Mensik J, Pospisil Z, Franz J, Dreslerova J (1971b): Local effect of passively acquired colostral antibody on the development of experimental swine influenza infection in suckling pigs. Zentralblatt Veterinärmedizin, Reihe B 18, 804-818. Go to original source... Go to PubMed...
  62. Mestecky J, Russell MW, Jackson S, Brown TA (1986): The human IgA system: a reassessment. Clinical Immunology and Immunopathology 40, 105-114. Go to original source... Go to PubMed...
  63. Minion FC, Adams C, Hsu T (2000): R1 region of P97 mediates adherence of Mycoplasma hyopneumoniae to swine cilia. Infection and Immunity 68, 3056-3060. Go to original source... Go to PubMed...
  64. Morgan KL, Hussein AM, Newby TJ, Bourne FJ (1980): Quantification and origin of the immunoglobulins in porcine respiratory tract secretions. Immunology 41, 729-736. Go to PubMed...
  65. Mostov K, Kaetzel CS (1999): Immunoglobulin transport and the polymeric immunoglobulin receptor. In: Ogra PL, Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR (eds.): Mucosal Immunology. 2nd ed. Academic Press, San Diego. 181-212.
  66. Nechvatalova K, Knotigova P, Krejci J, Faldyna M, Gopfert E, Satran P, Toman M (2005): Significance of different types and levels of antigen-specific immunity to Actinobacillus pleuropneumoniae infection in piglets. Veterinarni Medicina 50, 47-59. Go to original source...
  67. Nechvatalova K, Kudlackova H, Leva L, Babickova K, Faldyna M (2011): Transfer of humoral and cell-mediated immunity via colostrum in pigs. Veterinary Immunology and Immunopathology 142, 95-100. Go to original source... Go to PubMed...
  68. Ondrackova P, Nechvatalova K, Kucerova Z, Leva L, Dominguez J, Faldyna M (2010): Porcine mononuclear phagocyte subpopulations in the lung, blood and bone marrow: dynamics during inflammation induced by Actinobacillus pleuropneumoniae. Veterinary Research 41, 64. Go to original source... Go to PubMed...
  69. Pabst R (1990): Compartmentalization and kinetics of lymphoid cells in the lung. Regional Immunology 3, 62-71.
  70. Pabst R (1996): The respiratory immune system of pigs. Veterinary Immunology and Immunopathology 54, 191-195. Go to original source... Go to PubMed...
  71. Pabst R, Gehrke I (1990): Is the bronchus-associated lymphoid tissue (BALT) an integral structure of the lung in normal mammals, including humans? American Journal of Respiratory Cell and Molecular Biology 3, 131-135. Go to original source... Go to PubMed...
  72. Pabst R, Binns RM (1994): The immune system of the respiratory tract in pigs. Veterinary Immunology and Immunopathology 43, 151-156. Go to original source... Go to PubMed...
  73. Pabst R, Tschernig T (1995): Lymphocytes in the lung: an often neglected cell. Numbers, characterization and compartmentalization. Anatomy and Embryology 192, 293-299. Go to original source... Go to PubMed...
  74. Pruitt KM, Rahemtulla B, Rahemtulla F, Russell MW (1999): Innate humoral factors. In: Ogra PL, Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR (eds.): Mucosal Immunology. 2nd ed. Academic Press, San Diego. 65-88.
  75. Puci A, Clancy R, Jackson G (1982): Quantitation of Tlymphocyte subsets in human bronchus mucosa. The American Review of Respiratory Disease 126, 364-366. Go to PubMed...
  76. Reynolds HY (1991): Immunologic system in the respiratory tract. Physiological Reviews 71, 1117-1133. Go to original source... Go to PubMed...
  77. Reynolds HY, Merrill WW (1981): Airway changes in young smokers that may antedate chronic obstructive lung disease. Medical Clinics of North America 65, 667-689. Go to original source... Go to PubMed...
  78. Russell MW, Kilian M, Lamm ME (1999): Biological activities of IgA. In: Ogra PL, Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR (eds.): Mucosal Immunology. 2nd ed. Academic Press, San Diego. 225-251.
  79. Sedgwick JD, Holt PG (1985): Down-regulation of immune responses to inhaled antigen: studies on the mechanism of induced suppression. Immunology 56, 635-642. Go to PubMed...
  80. Sertl K, Takemura T, Tschachler E, Ferrans VJ, Kaliner MA, Shevach EM (1986): Dendritic cells with antigenpresenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. Journal of Experimental Medicine 163, 436-451. Go to original source... Go to PubMed...
  81. Schutte BC, McCray PB Jr. (2002): [beta]-Defensins in lung host defense. Annual Review of Physiology 64, 709-748. Go to original source... Go to PubMed...
  82. Stanley AC, Huntley JF, Jeffrey M, Buxton D (2001): Characterization of ovine nasal-associated lymphoid tissue and identification of M cells in the overlying follicle-associated epithelium. Journal of Comparative Pathology 125, 262-270. Go to original source... Go to PubMed...
  83. Summerfield A, McCullough KC (2009): The porcine dendritic cell family. Developmental and Comparative Immunology 33, 299-309. Go to original source... Go to PubMed...
  84. Travis SM, Conway BA, Zabner J, Smith JJ, Anderson NN, Singh PK, Greenberg EP, Welsh MJ (1999): Activity of abundant antimicrobials of the human airway. American Journal of Respiratory Cell and Molecular Biology 20, 872-879. Go to original source... Go to PubMed...
  85. van der Brugge-Gamelkoorn GJ, Claassen E, Sminia T (1986): Anti-TNP-forming cells in bronchus-associated lymphoid tissue (BALT) and paratracheal lymph node (PTLN) of the rat after intratracheal priming and boosting with TNP-KLH. Immunology 57, 405-409. Go to PubMed...
  86. von Garnier C, Nicod LP (2009): Immunology taught by lung dendritic cells. Swiss Medical Weekly 139, 186-192. Go to PubMed...
  87. Whary MT, Zarkower A, Confer FL, Ferguson FG (1995): Age-related differences in subset composition and activation responses of intestinal intraepithelial and mesenteric lymph node lymphocytes from neonatal swine. Cellular Immunology 163, 215-221. Go to original source... Go to PubMed...
  88. Winkler GC, Cheville NF (1987): Postnatal colonization of porcine lung capillaries by intravascular macrophages: an ultrastructural, morphometric analysis. Microvascular Research 33, 224-232. Go to original source... Go to PubMed...
  89. Yokomizo Y, Shimizu T (1979): Adherence of Bordetella bronchiseptica to swine nasal epithelial cells and its possible role in virulence. Research in Veterinary Sciences 27, 15-21. Go to original source...
  90. Zhang Q, Young TF, Ross RF (1994): Microtiter plate adherence assay and receptor analogs for Mycoplasma hyopneumoniae. Infection and Immunity 62, 1616-1622. Go to original source... Go to PubMed...
  91. Zhang G, Ross CR, Blecha F (2000): Porcine antimicrobial peptides: new prospects for ancient molecules of host defense. Veterinary Research 31, 277-296. Go to original source... Go to PubMed...

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