Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-25T09:05:17.805Z Has data issue: false hasContentIssue false
  • English
  • Français

A review of porcine tonsils in immunity and disease

Published online by Cambridge University Press:  28 February 2007

Dennis C. Horter ,
Kyoung-Jin Yoon  and
Jeffrey J. Zimmerman
Dennis C. Horter
Affiliation:
Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA
Kyoung-Jin Yoon
Affiliation:
Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA
Jeffrey J. Zimmerman*
Affiliation:
Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The porcine tonsils are a group of lymphoepithelial tissues located at the common openings of the gastrointestinal and respiratory tracts. The tonsils participate in a variety of functions involving innate, cellular and humoral immunity at the local and systemic levels. Among these immunological functions is the continuous surveillance for the presence of foreign antigens at the openings of the gastrointestinal and respiratory tracts. Within the pig, the movement of lymphocytes, cytokines and chemotactic molecules from the tonsils to other lymphoid organs confers immunity to other portals of pathogen entry and facilitates an efficient and rapid systemic immune response. In spite of the immunological nature of the tonsils, some microorganisms have acquired adaptations that allow them to circumvent the tonsillar immune defenses and utilize the tonsils as a site of entry, replication and colonization. Several bacterial and viral pathogens persist asymptomatically within the tonsils, making identification of asymptomatic carrier animals difficult in disease control and/or pathogen elimination. This paper reviews the current information on the anatomy, immunology and pathobiology of porcine tonsils and discusses the tonsils as a site of pathogen entry, replication and colonization using Salmonella spp., classical swine fever virus and porcine reproductive and respiratory syndrome virus as examples.

Keywords

tonsilsimmunitydiseasepigs
Type
Review Article
Information
Animal Health Research Reviews , Volume 4 , Issue 2 , December 2003 , pp. 143 - 155
Copyright
Copyright © CAB International 2003

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ackermann, MR, De Bey, MC, Register, KB, Larson, DJ and Kinyon, JM (1994). Tonsil and turbinate colonization by toxigenic and non-toxigenic strains of Pasteurella multocida in conventionally raised Iowa swine. Proceedings of the International Pig Veterinary Society 13: 162.Google Scholar
Albina, E, Madec, F, Cariolet, R and Torrison, J (1994). Immune response and persistence of the porcine reproductive and respiratory syndrome virus in infected pigs and farm units. Veterinary Record 134: 567–573.CrossRefGoogle ScholarPubMed
Alexandersen, S, Oleksiewicz, MB and Donaldson, AI (2001). The early pathogenesis of foot-and-mouth disease in pigs infected by contact: a quantitative time-course study using TaqMan RT–PCR. Journal of General Virology 82: 747–755.CrossRefGoogle ScholarPubMed
Allende, R, Laegreid, WW, Kutish, GF, Galeota, JA, Wills, RW and Osorio, FA (2000). Porcine reproductive and respiratory syndrome virus: description of persistence in individual pigs upon experimental infection. Journal of Virology 74: 10834–10837.CrossRefGoogle ScholarPubMed
Andries, K and Pensaert, M (1980). Immunofluorescence studies on the pathogenesis of hemagglutinating encephalomyelitis virus after oronasal inoculation. American Journal of Veterinary Research 41: 1372–1378.Google ScholarPubMed
Baekbo, P (1988). Pathogenic properties of Pasteurella multocida in the lung of pigs. Proceedings of the International Pig Veterinary Society 10: 58.Google Scholar
Baele, M, Chiers, K, Devriese, LA, Smith, HE, Wisselink, HJ, Vaneechoutte, M and Haesebrouck, F (2001). The gram-positive tonsillar and nasal flora of piglets before and after weaning. Journal of Applied Microbiology 91: 997–1003.CrossRefGoogle ScholarPubMed
Bagby, GC Jr, Rigas, VD, Bennett, RM, Vandenbark, AA and Garewal, HS (1981). Interaction of lactoferrin, monocytes, and T lymphocyte subsets in the regulation of steady-state granulopoiesis in vitro. Journal of Clinical Investigation 68: 56–63.CrossRefGoogle Scholar
Baskerville, A and Dow, C (1973). Pathology of experimental pneumonia in pigs produced by Salmonella choleraesuis. Journal of Comparative Pathology 83: 207–215.CrossRefGoogle Scholar
Bautista, EM and Molitor, TW (1997). Cell-mediated immunity to porcine reproductive and respiratory syndrome virus in swine. Viral Immunology 10: 83–94.CrossRefGoogle ScholarPubMed
Belz, GT (1998). Intercellular and lymphatic pathways associated with tonsils of the soft palate in young pigs. Anatomy and Embryology 197: 331–340.CrossRefGoogle ScholarPubMed
Belz, GT and Heath, TJ (1995). Lymphatic drainage from the tonsil of the soft palate in pigs. Journal of Anatomy 187: 491–495.Google ScholarPubMed
Belz, GT and Heath, TJ (1996). Tonsils of the soft palate of young pigs: crypt structure and lymphoepithelium. Anatomical Record 245: 102–113.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Bennell, MA and Husband, AJ (1981). Route of lymphocyte migration in pigs. I. Lymphocyte circulation in gut-associated lymphoid tissue. Immunology 42: 469–474.Google ScholarPubMed
Beyer, J, Fichtner, D, Schirrmeier, H, Polster, U, Weiland, E and Wege, H (2000). Porcine reproductive and respiratory syndrome virus (PRRSV): kinetics of infection in lymphatic organs and lung. Journal of Veterinary Medicine B, Infectious Diseases And Veterinary Public Health 47: 9–25.CrossRefGoogle ScholarPubMed
Bianchi, AT, Zwart, RJ, Jeurissen, SH and Moonen-Leusen, HW (1992). Development of the B- and T-cell compartments in porcine lymphoid organs from birth to adult life: an immunohistological approach. Veterinary Immunology and Immunopathology 33: 201–221.CrossRefGoogle Scholar
Binns, RM and Hall, JG (1966). The paucity of lymphocytes in the lymph of unanaesthetized pigs. British Journal of Experimental Pathology 47: 275–280.Google Scholar
Binns, RM and Pabst, R (1988). Lymphoid cell migration and homing in the young pig: alternative immune mechanisms in action. In: Husband, A (editor). Migration and Homing of Lymphoid Cells. Boca Raton: CRC Press, pp. 137–174.Google Scholar
Boeker, M, Pabst, R and Rothkotter, J (1999). Quantification of B, T and null lymphocyte subpopulations in the blood and lymphoid organs of the pig. Immunobiology 201: 74–87.CrossRefGoogle Scholar
Borror, DJ (1971). Dictionary of Word Roots and Combining Forms. Palo Alto (CA): Mayfield Publishing Company.Google Scholar
Brandtzaeg, P, Baekkefold, ES, Farstad, IN, Jahnsen, FL, Johanson, FE, Nilsen, EM and Yamanaka, T (1999). Regional specialization in the mucosal immune system: what happens in the microcompartments? Immunology Today 20: 141–151.CrossRefGoogle ScholarPubMed
Brown, TT Jr, Shin, KO and Fuller, FJ (1995). Detection of pseudorabies viral DNA in tonsillar epithelial cells of latently infected pigs. American Journal of Veterinary Research 56: 587–594.CrossRefGoogle ScholarPubMed
CDC (2001). Preliminary FoodNet data on the incidence of foodborne illnesses—selected sites, United States, 2000. Morbidity and Mortality Weekly Report 50: 241–246.Google Scholar
Cheville, NF and Mengeling, WL (1969). The pathogenesis of chronic hog cholera (swine fever): histologic, immunofluorescent, and electron microscopic studies. Laboratory Investigations 20: 261–274.Google ScholarPubMed
Choi, C and Chae, C (2003). Detection of classical swine fever virus in boar semen by reverse transcription–polymerase chain reaction. Journal of Veterinary Diagnostic Investigations 15: 35–41.CrossRefGoogle ScholarPubMed
Colgrove, G, Haelterman, EO and Coggins, L (1969). Pathogenesis of African swine fever virus in young pigs. American Journal of Veterinary Research 30: 1343–1359.Google ScholarPubMed
Cooper, NR (1985). The classical complement pathway. Activation and regulation of the first complement component. Advances in Immunology 37: 151–216.CrossRefGoogle ScholarPubMed
Darwich, L, Segales, J, Domingo, M and Mateu, E (2002). Changes in CD4(+), CD8(+), CD4(+), CD8(+), and immunoglobulin M-positive peripheral blood mononuclear cells of postweaning multisystemic wasting syndrome-affected pigs and age-matched uninfected wasted and healthy pigs correlate with lesions and porcine circovirus type 2 load in lymphoid tissues. Clinical and Diagnostic Laboratory Immunology 9: 236–42.Google ScholarPubMed
Davies, PR and Ossowicz, CJ (1991). Evaluation of methods used for detecting Streptococcus suis type 2 in tonsils, and investigation of the carrier state in pigs. Research in Veterinary Science 50: 190–194.CrossRefGoogle ScholarPubMed
de Jong, MF, Wellenberg, G, Schaake, J and Frik, K (1988). Selection of pig breeding herds free from atrophic rhinitis by means of a bacteriological screening of pigs on DNT producing Pasteurella multocida: a field evaluation from 1981 until 1987. Proceedings of the International Pig Veterinary Society 10: 49.Google Scholar
Dekker, A, Moonen, P, de Boer-Luijtze, EA and Terpstra, C (1995). Pathogenesis of swine vesicular disease after exposure of pigs to an infected environment. Veterinary Microbiology 45: 243–50.CrossRefGoogle Scholar
Devriese, LA, Hommez, J, Pot, B and Haesebrouck, F (1994). Identification and composition of the streptococcal and enterococcal flora of tonsils, intestines and faeces of pigs. Journal of Applied Bacteriology 77: 31–36.CrossRefGoogle ScholarPubMed
Dick, CP, Johnson, RP and Yamashiro, S (1989). Sites of persistence of feline calicivirus. Research in Veterinary Science 47: 367–73.CrossRefGoogle ScholarPubMed
Dillender, MJ and Lunney, JK (1993). Characteristics of T lymphocyte cell lines established from NIH minipigs challenge inoculated with Trichinella spiralis. Veterinary Immunology and Immunopathology 35: 301–319.CrossRefGoogle ScholarPubMed
Dunne, HW (1973). Hog cholera (European swine fever). Advances in Veterinary Science and Comparative Medicine 17: 315–359.Google ScholarPubMed
Edwards, S, Fukusho, A, Lefevre, P-C, Lipowski, A, Pejsak, Z, Roehe, P and Westergaard, J (2000). Classical swine fever: The global situation. Veterinary Microbiology 73: 103–119.CrossRefGoogle ScholarPubMed
Ellis, J, Hassard, L, Clark, E, Harding, J, Allan, G, Willson, P, Strokappe, J, Martin, K, McNeilly, F, Meehan, B, Todd, D and Haines, D (1998). Isolation of circovirus from lesions of pigs with postweaning multisystemic wasting syndrome. Canadian Veterinary Journal 39: 44–51.Google ScholarPubMed
Elvinger, F, Liggett, AD, Tang, KN, Harrison, LR, Cole, JR Jr, Baldwin, CA and Nessmith, WB (1994). Eastern equine encephalomyelitis virus infection in swine. Journal of the American Veterinary Medical Association 205: 1014–1016.CrossRefGoogle ScholarPubMed
Fedorka-Cray, PJ, Whipp, SC, Isaacson, RE, Nord, N and Lager, K (1994). Transmission of Salmonella typhimurium to swine. Veterinary Microbiology 41: 333–344.CrossRefGoogle ScholarPubMed
Fedorka-Cray, PJ, Kelley, LC, Stabel, TJ, Gray, JT and Laufer, JA (1995). Alternate routes of invasion may affect pathogenesis of Salmonella typhimurium. Infection and Immunity 63: 2658–2664.CrossRefGoogle ScholarPubMed
Fleming, A (1922). On a remarkable bacteriolytic element found in tissues and secretions. Proceedings of the Royal Society of London Series B 93: 306–317.Google Scholar
Fu, Y and Galan, JE (1999). A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401: 293–297.CrossRefGoogle ScholarPubMed
Gram, T, Ahrens, P and Nielsen, JP (1996). Evaluation of a PCR for detection of Actinobacillus pleuropneumoniae in mixed bacterial cultures from tonsils. Veterinary Microbiology 51: 95–104.CrossRefGoogle ScholarPubMed
Gray, JT, Fedorka-Cray, PJ, Stabel, TJ and Ackermann, MR (1995). Influence of inoculation route on the carrier state of Salmonella choleraesuis in swine. Veterinary Microbiology 47: 43–59.CrossRefGoogle ScholarPubMed
Hancock, RE and Scott, MG (2000). The role of antimicrobial peptides in animal defenses. Proceedings of the National Academy of Sciences of the United States of America 97: 8856–8861.CrossRefGoogle ScholarPubMed
Hardy, GA, Imami, N and Gotch, FM (2002). Improving HIV-specific immune responses in HIV-infected patients. Journal of HIV Therapy 7: 40–45.Google ScholarPubMed
Harms, PA, Sorden, SD, Halbur, PG, Bolin, SR, Lager, KM, Morozov, I and Paul, PS (2001). Experimental reproduction of severe disease in CD/CD pigs concurrently infected with type 2 porcine circovirus and porcine reproductive and respiratory syndrome virus. Veterinary Pathology 38: 528–539.CrossRefGoogle ScholarPubMed
Higgins, R and Gottschalk, M (1999). Streptococcal diseases. In: Straw, BE, D'Allaire, S, Mengeling, WL and Taylor, DJ (editors). Diseases of Swine. 8th edn. Ames (IA): Iowa State Press pp. 563–578.Google Scholar
Horter, DC, Pogranichniy, RM, Chang, CC, Evans, RB, Yoon, KJ and Zimmerman, JJ (2002). Characterization of the carrier state in porcine reproductive and respiratory syndrome virus infection. Veterinary Microbiology 86: 213–28.CrossRefGoogle ScholarPubMed
Howerth, EW, Stallknecht, DE, Dorminy, M, Pisell, T and Clarke, GR (1997). Experimental vesicular stomatitis in swine: effects of route of inoculation and steroid treatment. Journal of Veterinary Diagnostic Investigations 9: 136–142.CrossRefGoogle ScholarPubMed
Howie, AJ (1981). The cells in tonsillar crypts. Clinical Otolaryngology and Allied Sciences 7: 35–44.CrossRefGoogle Scholar
Kassay, D and Sandor, A (1962). The crypt system of the palatine tonsils. Archives of Otolaryngology 75: 144–155.CrossRefGoogle ScholarPubMed
Kleiboeker, SB, Lehman, JR and Fangman, TJ (2002). Concurrent use of reverse transcription–polymerase chain reaction testing of oropharyngeal scrapings and paired serological testing for detection of porcine reproductive and respiratory syndrome virus infection in sows. Journal of Swine Health and Production 10: 251–258.Google Scholar
Kotenko, SV, Saccani, S, Izotova, LS, Mirochnitchenko, OV and Pestka, S (2000). Human cytomegalovirus harbors its own unique IL-10 homologue (cmvIL-10). Proceedings of the National Academy of Sciences of the United States of America 97: 1695–1700.CrossRefGoogle Scholar
Krmpoti, A, Busch, DH, Bubi, I, Gebhardt, F, Hengel, H, Hasan, M, Scalzo, AA, Koszinowski, UH and Jonji, S (2002). MCMV glycoprotein gp40 confers virus resistance to CD8+ T cells and NK cells in vivo. Nature Immunology 3: 529–535.CrossRefGoogle Scholar
Kume, K, Nakai, T and Sawata, A (1984). Isolation of Haemophilus pleuropneumoniae from the nasal cavities of healthy pigs. Japanese Journal of Veterinary Science 46: 641–647.Google ScholarPubMed
Kwapinski, JBG (1972). Methodology of Immunochemical and Immunological Research. New York: John Wiley and Sons pp. 609–611.Google Scholar
Laufer, J, Oren, R, Goldberg, I, Horwitz, A, Kopolovic, J, Chowers, Y and Passwell, JH (2000). Cellular localization of complement C3 and C4 transcripts in intestinal specimens from patients with Crohn's disease. Clinical Experimental Immunology 120: 30–37.CrossRefGoogle ScholarPubMed
Levitskaya, J, Coram, M, Levitsky, V, Imreh, S, Steigerwald-Mullen, PM, Klein, G, Kurilla, MG and Masucci, MG (1995). Inhibition of antigen processing by the internal repeat region of the Epstein–Barr virus nuclear antigen 1. Nature 375: 685–688.CrossRefGoogle ScholarPubMed
Levitskaya, J, Sharipo, A, Leonchiks, A, Ciechanover, A and Masucci, MG (1997). Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein–Barr virus nuclear antigen 1. Proceedings of the National Academy of Sciences of the United States of America 94: 12616–12621.CrossRefGoogle ScholarPubMed
Loemba, HD, Mounir, S, Mardassi, H, Archambault, D and Dea, S (1996). Kinetics of humoral immune response to the major structural proteins of the porcine reproductive and respiratory syndrome virus. Archives of Virology 141: 751–761.CrossRefGoogle Scholar
Long, JF (1985). Pathogenesis of porcine polioencephalomyelitis. In: Olsen, RA, Krakowka, S and Blakeslee, JR (editors). Comparative Pathobiology of Viral Diseases, Vol. 1. Boca Raton (FL): CRC Press pp. 179–197.Google Scholar
Madsen, LW, Svensmark, B, Elvestad, K, Aalbaek, B and Jensen, HE (2002). Streptococcus suis serotype 2 infection in pigs: new diagnostic and pathogenetic aspects. Journal of Comparative Pathology 126: 57–65.CrossRefGoogle ScholarPubMed
McClurkin, AW, Littledike, ET, Cutlip, RC, Frank, GH, Coria, MF and Bolin, SR (1984). Production of cattle immunotolerant to bovine viral diarrhea virus. Canadian Journal of Comparative Medicine 48: 156–161.Google ScholarPubMed
Meyerholz, DK, Stabel, TJ, Ackermann, MR, Carlson, SA, Jones, BD and Pohlenz, J (2002). Early epithelial invasion by Salmonella enterica serovar Typhimurium DT104 in the swine ileum. Veterinary Pathology 39: 712–720.CrossRefGoogle ScholarPubMed
Morozov, I, Sirinarumitr, T, Sorden, SD, Halbur, PG, Morgan, MK, Yoon, KJ and Paul, PS (1998). Detection of a novel strain of porcine circovirus in pigs with postweaning multisystemic wasting syndrome. Journal of Clinical Microbiology 36: 2535–2541.CrossRefGoogle ScholarPubMed
Murakami, S, Azuma, R, Koeda, T, Oomi, H, Watanabe, T and Fujiwara, H (1998). Immunohistochemical detection for Actinomyces sp. in swine tonsillar abscess and granulomatous mastitis. Mycopathologia 141: 15–9.CrossRefGoogle ScholarPubMed
Neutra, MR, Pringault, E and Kraehenbuhl, JP (1996). Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annual Review of Immunology 14: 275–300.CrossRefGoogle ScholarPubMed
Nielsen, B, Heisel, C and Wingstrand, A (1996). Time course of the serological response to Yersinia enterocolitica O:3 in experimentally infected pigs. Veterinary Microbiology 48: 293–303.CrossRefGoogle ScholarPubMed
Pabst, R and Binns, RM (1989). Heterogeneity of lymphocyte homing physiology: several mechanisms operate in the control of migration to lymphoid and non-lymphoid organs in vivo. Immunology Reviews 108: 83–109.CrossRefGoogle ScholarPubMed
Pabst, R and Nowara, E (1984). The emigration of lymphocytes from palatine tonsils after local labeling. Archives of Otorhinolaryngology 240: 7–13.CrossRefGoogle Scholar
Pantaleo, G, Graziosi, C, Butini, L, Pizzo, PA, Schnittman, SM, Kotler, DP and Fauci, AS (1991). Lymphoid organs function as major reservoirs for human immunodeficiency virus. Proceedings of the National Academy of Sciences of the United States of America 88: 9838–9842.CrossRefGoogle ScholarPubMed
Paton, D (2002). The reappearance of classical swine fever in England in 2000. In: Morilla, A, Yoon, K-J and Zimmerman, JJ (editors). Trends in Emerging Viral Infections of Swine. Ames (IA): Iowa State Press pp. 153–158.CrossRefGoogle Scholar
Payne, JM and Derbyshire, JB (1963). Portals of entry for bacterial infection in calves and piglets with particular reference to the tonsil. Journal of Pathology and Bacteriology 85: 171–178.CrossRefGoogle Scholar
Payne, S, Parekh, B, Montelaro, RC and Issel, CJ (1984). Genomic alterations associated with persistent infections by equine infectious anaemia virus, a retrovirus. Journal of General Virology 65: 1395–1399.CrossRefGoogle ScholarPubMed
Perry, ME (1994). The specialized structure of crypt epithelium in the human palatine tonsil and its functional significance. Journal of Anatomy 185: 111–127.Google ScholarPubMed
Pescovitz, MD, Sakopoulos, AG, Gaddy, JA, Husmann, RJ and Zuckermann, FA (1994). Porcine peripheral blood CD4+/CD8+ dual expressing T-cells. Veterinary Immunology and Immunopathology 43: 53.CrossRefGoogle ScholarPubMed
Ploegh, HL (1998). Viral strategies of immune evasion. Science 280: 248–53.CrossRefGoogle ScholarPubMed
Pospischil, A, Wood, RL and Anderson, TD (1990). Peroxidase-antiperoxidase and immunogold labeling of Salmonella typhimurium and Salmonella choleraesuis var kunzendorf in tissues of experimentally infected swine. American Journal of Veterinary Research 51: 619–624.CrossRefGoogle ScholarPubMed
Rabsch, W, Tschape, H and Baumler, AJ (2001). Non-typhoidal salmonellosis: emerging problems. Microbes and Infection 3: 237–247.CrossRefGoogle ScholarPubMed
Ramos, JA, Ramis, AJ, Rabanal, RM, Marco, A, Domingo, M and Ferrer, LM (1990). Scanning electron microscopy of swine lymphoid organs. Histology and Histopathology 5: 397–406.Google ScholarPubMed
Ramos, JA, Ramis, AJ, Marco, A, Domingo, M, Rabanal, R and Ferrer, L (1992). Histochemical and immunohistochemical study of the mucosal lymphoid system in swine. American Journal of Veterinary Research 53: 1418–1426.CrossRefGoogle ScholarPubMed
Ressang, AA (1973). Studies on the pathogenesis of hog cholera. I. Demonstration of hog cholera virus subsequent to oral exposure. Zentralblatt für Veterinärmedizin 20: 256–271.CrossRefGoogle ScholarPubMed
Robertson, A, Bannister, GL, Boulanger, P, Appel, M and Gray, DP (1965). Hog cholera. V. Demonstration of the antigen in swine tissues by the fluorescent antibody technique. Canadian Journal of Comparative Medicine and Veterinary Science 29: 299–305.Google ScholarPubMed
Rossow, KD, Benfield, DA, Goyal, SM, Nelson, EA, Christopher-Hennings, J and Collins, JE (1996). Chronological immunohistochemical detection and localization of porcine reproductive and respiratory syndrome virus in gnotobiotic pigs. Veterinary Pathology 33: 551–556.CrossRefGoogle ScholarPubMed
Rutter, JM (1985). Atrophic rhinitis in swine. Advances in Veterinary Science and Comparative Medicine 29: 239–279.Google ScholarPubMed
Saalmuller, A, Redehasse, MJ, Buhring, HJ, Jonjic, S and Koszinowski, UH (1987). Simultaneous expression of CD4 and CD8 antigens by a substantial proportion of resting porcine T lymphocytes. European Journal of Immunology 17: 1297.CrossRefGoogle ScholarPubMed
Saar, LI and Getty, R (1964). The interrelationship of the lymph vessel connections of the lymph nodes of the head, neck, and shoulder regions of swine. American Journal of Veterinary Research 25: 618–636.Google ScholarPubMed
Sahasrabudhe, KS, Kimball, JR, Morton, TH, Weinberg, A and Dale, BA (2000). Expression of the antimicrobial peptide, human beta-defensin 1, in duct cells of minor salivary glands and detection in saliva. Journal of Dental Research 79: 1669–1677.CrossRefGoogle ScholarPubMed
Salles, MW and Middleton, DM (2000). Lymphocyte subsets in porcine tonsillar crypt epithelium. Veterinary Immunology and Immunopathology 77: 133–144.CrossRefGoogle ScholarPubMed
Salles, MW, Perez-Casal, J, Willson, P and Middleton, DM (2002). Changes in the leucocyte subpopulations of the palatine tonsillar crypt epithelium of pigs in response to Streptococcus suis type 2 infection. Veterinary Immunology and Immunopathology 87: 51–63.CrossRefGoogle ScholarPubMed
Sallusto, F, Lanzavecchia, A and Mackay, CR (1998). Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunology Today 19: 568–574.CrossRefGoogle ScholarPubMed
Salmon, DE (1889). Hog cholera: its history, nature, and treatment. Washington: Bureau of Animal Industry, US Department of Agriculture, Washington Printing Office, p. 32.Google Scholar
Sato, Y, Wake, K and Watanabe, I (1990). Differentiation of crypt epithelium in human palatine tonsils: the microenvironment of crypt epithelium as a lymphoepithelial organ. Archives of Histology and Cytology 53: 41–54.CrossRefGoogle ScholarPubMed
Schummer, A and Nickel, R (1979). Digestive system. In: Sack, WO (editor). The Viscera of the Domestic Mammals, 2nd edn. Berlin: Springer-Verlag pp. 51–55.Google Scholar
Senkevich, TG, Bugert, JJ, Sisler, JR, Koonin, EV, Darai, G and Moss, B (1996). Genome sequence of a human tumorigenic poxvirus: prediction of specific host-response-evasion genes. Science 273: 813–816.CrossRefGoogle ScholarPubMed
Shadduck, JA, Koestner, A and Kasza, L (1967). The lesions of porcine adenoviral infection in germfree and pathogen-free pigs. Pathologia Veterinaria 4: 537–552.CrossRefGoogle ScholarPubMed
Sharipo, A, Imreh, M, Leonchiks, A, Brändén, C-I and Masucci, MG (2001). cis-Inhibition of proteasomal degradation by viral repeats: impact of length and amino acid composition. FEBS Letters 499: 137–142.CrossRefGoogle ScholarPubMed
Shi, J, Zhang, G, Wu, H, Ross, C, Blecha, F and Ganz, T (1999). Porcine epithelial beta-defensin 1 is expressed in the dorsal tongue at antimicrobial concentrations. Infection and Immunity 67: 3121–3127.CrossRefGoogle ScholarPubMed
Slipka, J (1988). Palatine tonsils—their evolution and ontogeny. Acta Oto-laryngologica 454: 18–22.CrossRefGoogle ScholarPubMed
Solorzano, RF, Thigpen, JE, Bedell, DM and Schwartz, WL (1966). The diagnosis of hog cholera by a fluorescent antibody test. Journal of the American Veterinary Medical Association 149: 31–34.Google ScholarPubMed
Stephano, AH, Gay, GM and Ramirez, TC (1988). Encephalomyelitis, reproductive failure and corneal opacity in pigs, associated with a new paramyxovirus infection (blue eye). Veterinary Record 122: 6–10.CrossRefGoogle Scholar
Terpstra, C and Wensvoort, G (1988). Bovine viral diarrhea virus infections in piglets born to sows vaccinated against swine fever with contaminated vaccine. Research in Veterinary Science 45: 143–148.CrossRefGoogle Scholar
Terpstra, C and de Smit, AJ (2000). The 1997/1998 epizootic of swine fever in the Netherlands: control strategies under a non-vaccination regimen. Veterinary Microbiology 77: 3–15.CrossRefGoogle Scholar
Terpstra, C, Wensvoort, G and Pol, JMA (1991). Experimental reproduction of porcine epidemic abortion and respiratory syndrome (mystery swine disease) by infection with Lelystad virus: Koch's postulates fulfilled. Veterinary Quarterly 13: 131–136.CrossRefGoogle ScholarPubMed
Terzic, S, Sver, L, Valpotic, I, Lojkic, M, Miletic, Z, Jemersic, L, Lackovic, G, Kovsca-Janjatovic, A and Orsolic, N (2002). Immunophenotyping of leukocyte subsets in peripheral blood and palatine tonsils of prefattening pigs. Veterinary Research Communications 26: 273–283.CrossRefGoogle ScholarPubMed
Thibodeau, V, Frost, EH, Chenier, S and Quessy, S (1999). Presence of Yersinia enterocolitica in tissues of orally-inoculated pigs and the tonsils and feces of pigs at slaughter. Canadian Journal of Veterinary Research 63: 96–100.Google ScholarPubMed
Trautmann, A and Fiebiger, J (1957). Fundamentals of the Histology of Domestic Animals. Ithaca (NY): Comstock Publishing Associates pp. 121–123.Google Scholar
Uchiya, K, Barbieri, MA, Funato, K, Shah, AH, Stahl, PD and Groisman, EA (1999). A Salmonella virulence protein that inhibits cellular trafficking. EMBO Journal 18: 3924–3933.CrossRefGoogle ScholarPubMed
Van Oirschot, JT and Terpstra, C (1977). A congenital persistent swine fever infection. I. Clinical and virological observations. Veterinary Microbiology 2: 121–132.CrossRefGoogle Scholar
Velinova, M, Thielen, C, Melot, F, Donga, J, Eicher, S, Heinen, E and Antoine, N (2001). New histochemical and ultrastructural observations on normal bovine tonsils. Veterinary Record 149: 613–617.CrossRefGoogle ScholarPubMed
Wensvoort, G, Terpstra, C, Pol, JM, ter Laak, EA, Bloemraad, M, de Kluyver, EP, Kragten, C, van Buiten, L, den Besten, A and Wagenaar, F (1991). Mystery swine disease in the Netherlands: the isolation of Lelystad virus. Veterinary Quarterly 13: 121–130.CrossRefGoogle ScholarPubMed
Wheeler, JG and Osorio, FA (1991). Investigation of sites of pseudorabies virus latency, using polymerase chain reaction. American Journal of Veterinary Research 52: 1799–1803.CrossRefGoogle ScholarPubMed
Wilcock, BP and Olander, HJ (1978). Influence of oral antibiotic feeding on the duration and severity of clinical disease, growth performance and pattern of shedding in swine inoculated with Salmonella typhimurium. Journal of the American Veterinary Medical Association 172: 472–477.Google ScholarPubMed
Wilcock, BP, Armstrong, CH and Olander, HJ (1976). The significance of the serotype in the clinical and pathologic features of naturally occurring porcine salmonellosis. Canadian Journal of Comparative Medicine 40: 80–88.Google ScholarPubMed
Williams, DM and Rowland, AC (1972). The palatine tonsils of the pig—an efferent route to the lymphoid tissue. Journal of Anatomy 113: 131–137.Google Scholar
Williams, DM, Lawson, GHK and Rowland, AC (1973). Streptococcal infection in piglets: the palatine tonsil as portals of entry for Streptococcus suis. Research in Veterinary Science 15: 352–362.CrossRefGoogle ScholarPubMed
Wills, RW, Zimmerman, JJ, Yoon, KJ, Swenson, SL, McGinley, MJ, Hill, HT, Platt, KB, Christopher-Hennings, J and Nelson, EA (1997). Porcine reproductive and respiratory syndrome virus: a persistent infection. Veterinary Microbiology 55: 231–240.CrossRefGoogle ScholarPubMed
Winkler, MT, Doster, A and Jones, C (2000). Persistence and reactivation of bovine herpesvirus 1 in the tonsils of latently infected calves. Journal of Virology 74: 5337–5346.CrossRefGoogle ScholarPubMed
Wood, RL and Rose, R (1992). Populations of Salmonella typhimurium in internal organs of experimentally infected carrier swine. American Journal of Veterinary Research 53: 653–658.CrossRefGoogle ScholarPubMed
Wood, RL, Pospischil, A and Rose, R (1989). Distribution of persistent Salmonella typhimurium infection in internal organs of swine. American Journal of Veterinary Research 50: 1015–1021.Google ScholarPubMed
Wu, AM, Csako, G and Herp, A (1994). Structure, biosynthesis, and function of salivary mucins. Molecular and Cellular Biochemistry 17: 39–55.CrossRefGoogle Scholar
Yamamoto, Y, Okato, S, Nishiyama, M and Takahashi, H (1992). Function and morphology of macrophages in palatine tonsils. Advances in Otorhinolaryngology 47: 107–113.Google ScholarPubMed
Zhang, G, Ross, CR and Blecha, F (2000). Porcine antimicrobial peptides: new prospects for ancient molecules of host defense. Veterinary Research 31: 277–296.CrossRefGoogle ScholarPubMed
Zimmerman, JJ (2003). Historical overview. In: Zimmerman, JJ and Yoon, K-J (editors). The Porcine Reproductive and Respiratory Syndrome (Porcine Arterivirus) Compendium 2nd edn. Des Moines (IA): National Pork Board pp. 1–6.Google Scholar
Zimmerman, JJ, Sanderson, T, Eernisse, KA, Hill, HT and Frey, ML (1992). Transmission of SIRS virus in convalescent animals to commingled penmates under experimental conditions. American Association Swine Practitioners Newsletter 4: 25.Google Scholar
Zuckermann, FA (1999). Extrathymic CD4/CD8 double positive T cells. Veterinary Immunology and Immunopathology 72: 55–66.CrossRefGoogle ScholarPubMed
Zuckermann, FA and Gaskins, HR (1996). Distribution of porcine CD4/CD8 double-positive T lymphocytes in mucosa-associated lymphoid tissues. Immunology 87: 493–499.CrossRefGoogle ScholarPubMed
Zuckermann, FA and Husmann, RJ (1996). Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology 87: 500–512.Google ScholarPubMed
Zwirner, J, Felber, E, Schmidt, P, Riethmuller, G and Feucht, HE (1989). Complement activation in human lymphoid germinal centres. Immunology 66: 270–277.Google ScholarPubMed