Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-01T21:09:42.765Z Has data issue: false hasContentIssue false

The microbiome of the soft palate of swine

Published online by Cambridge University Press:  04 July 2012

Shaun Kernaghan
Affiliation:
Department of Pathobiology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
Adina R. Bujold
Affiliation:
Department of Pathobiology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
Janet I. MacInnes*
Affiliation:
Department of Pathobiology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
*
*Corresponding author. E-mail: macinnes@uoguelph.ca

Abstract

The tonsil of the soft palate in pigs is a secondary lymphoid tissue that provides a first line of defense against foreign antigens entering by the mouth or nares. It has been known for a long time to be the site of colonization of important swine and zoonotic bacterial pathogens. Initially our understanding of microbes present at this site came from culture-based studies. Very recently, sequence-based approaches have been used to identify the core microbiome of the swine tonsil. Although animal to animal and herd to herd variation was detected in these studies, >90 of the organisms detected belonged to the phyla Proteobacteria and Firmicutes. Members of the family Pasteurellaceae appeared to be predominate in the tonsil; however, the relative proportions of Actinobacillus, Haemophilus, and Pasteurella varied. Members of the families Moraxellaceae, Fusobacteriaceae, Veillonellaceae, and Neisseriaceae were also seen as frequent residents of the tonsil.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2012

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

Aas, JA, Paster, BJ, Stokes, LN, Olsen, I and Dewhirst, FE (2005). Defining the normal bacterial flora of the oral cavity. Journal of Clinical Microbiology 43: 57215732.Google Scholar
Aas, JA, Griffen, AL, Dardis, SR, Lee, AM, Olsen, I, Dewhirst, FE, Leys, EJ and Paster, BJ (2008). Bacteria of dental caries in primary and permanent teeth in children and young adults. Journal of Clinical Microbiology 46: 14071417.CrossRefGoogle ScholarPubMed
Autio, T, Markkula, A, Hellstrom, S, Niskanen, T, Lunden, J and Korkeala, H (2004). Prevalence and genetic diversity of Listeria monocytogenes in the tonsils of pigs. Journal of Food Protection 67: 805808.CrossRefGoogle ScholarPubMed
Avila, M, Ojcius, DM and Yilmaz, O (2009). The oral microbiota: living with a permanent guest. DNA and Cell Biology 28: 405411.CrossRefGoogle ScholarPubMed
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
Belz, GT and Heath, TJ (1996). Tonsils of the soft palate of young pigs: crypt structure and lymphoepithelium. Anatomical Record 245: 102113.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Brandtzaeg, P (2003). Immunology of tonsils and adenoids: everything the ENT surgeon needs to know. International Journal of Pediatric Otorhinolaryngology 67: S69S76.CrossRefGoogle ScholarPubMed
Brandtzaeg, P, Baekkevold, ES, Farstad, IN, Jahnsen, FL, Johansen, FE, Nilsen, EM and Yamanaka, T (1999). Regional specialization in the mucosal immune system: what happens in the microcompartments? Immunology Today 20: 141151.Google Scholar
Casteleyn, C, Breugelmans, S, Simoens, P and Van den Broeck, W (2011a). The tonsils revisited: review of the anatomical localization and histological characteristics of the tonsils of domestic and laboratory animals. Clinical and Developmental Immunology 2011: 472460.Google Scholar
Casteleyn, C, Simoens, P and Van den Broeck, W (2011b). Terminology of the tonsils. Anatomia, Histologia, Embryologia 40: 204209.Google Scholar
Chen, T, Yu, WH, Izard, J, Baranova, OV, Lakshmanan, A and Dewhirst, FE (2010). The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database: The Journal of Biological Databases and Curation 2010: baq013.Google Scholar
Chiers, K, Haesebrouck, F, Mateusen, B, Van Overbeke, I and Ducatelle, R (2001). Pathogenicity of Actinobacillus minor, Actinobacillus indolicus and Actinobacillus porcinus strains for gnotobiotic piglets. Journal of Veterinary Medicine B, Infectious Diseases and Veterinary Public Health 48: 127131.Google 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: 3136.CrossRefGoogle ScholarPubMed
Ellsworth, S, Kirkbride, CA and Johnson, DD (1980). Excretion of Mycobacterium avium from lesions in the intestine and tonsils of infected swine. American Journal of Veterinary Research 41: 15261530.Google ScholarPubMed
FAO/WHO (2002). Report of a joint FAO/WHO expert consultation on guidelines for the evaluation of probiotics in food. London, Ontario, Canada: World Health Organization and Food and Agriculture Organization of the United Nations.Google Scholar
Fredriksson-Ahomaa, M, Wacheck, S, Koenig, M, Stolle, A and Stephan, R (2009). Prevalence of pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis in wild boars in Switzerland. International Journal of Food Microbiology 135: 199202.Google Scholar
Guglielmetti, S, Taverniti, V, Minuzzo, M, Arioli, S, Stuknyte, M, Karp, M and Mora, D (2010). Oral bacteria as potential probiotics for the pharyngeal mucosa. Applied and Environmental Microbiology 76: 39483958.Google Scholar
Horter, DC, Yoon, KJ and Zimmerman, JJ (2003). A review of porcine tonsils in immunity and disease. Animal Health Research Reviews/Conference of Research Workers in Animal Diseases 4: 143155.CrossRefGoogle ScholarPubMed
Huyghebaert, G, Ducatelle, R and Van Immerseel, F (2011). An update on alternatives to antimicrobial growth promoters for broilers. Veterinary Journal 187: 182188.CrossRefGoogle ScholarPubMed
Jahnsen, FL and Brandtzaeg, P (1999). Antigen presentation and stimulation of the immune system in human airways. Allergy 54(Suppl. 57): 3749.CrossRefGoogle ScholarPubMed
Jamin, A, Gorin, S, Le Potier, M and Kuntz-Simon, G (2006). Characterization of conventional and plasmacytoid dendritic cells in swine secondary lymphoid organs and blood. Veterinary Immunology and Immunopathology 114: 224237.Google Scholar
Jensen, TK, Møller, K, Lindecrona, R and Jorsal, SE (2000). Detection of Lawsonia intracellularis in the tonsils of pigs with proliferative enteropathy. Research in Veterinary Science 68: 2326.Google Scholar
Kasenõmm, P, Kull, M and Mikelsaar, M (2002). Association between tonsillar core microflora and post-tonsillectomy bacteremia. Microbial Ecology in Health and Disease 14: 122127.CrossRefGoogle Scholar
Kenny, M, Smidt, H, Mengheri, E and Miller, B (2011). Probiotics – do they have a role in the pig industry? Animal: An International Journal of Animal Bioscience 5: 462470.Google Scholar
Kernaghan, S, Ojha, S, Slavic, D, Chen, S, Poljak, Z and MacInnes, JI (2011). Bacterial community profiling of tonsils from diseased pigs using terminal restriction fragment length polymorphism analysis. In 92nd AGM Conference of Research Workers in Animal Diseases, 92nd AGM Conference of Research Workers in Animal Diseases, Chicago, Illinois, December 4–6, 2011.Google Scholar
Lomonaco, S, Decastelli, L, Bianchi, DM, Nucera, D, Grassi, MA, Sperone, V and Civera, T (2009). Detection of Salmonella in finishing pigs on farm and at slaughter in Piedmont, Italy. Zoonoses and Public Health 56: 137144.Google Scholar
Lowe, BA, Marsh, TL, Isaacs-Cosgrove, N, Kirkwood, RN, Kiupel, M and Mulks, MH (2011). Microbial communities in the tonsils of healthy pigs. Veterinary Microbiology 147: 346357.Google Scholar
Lowe, BA, Marsh, TL, Isaacs-Cosgrove, N, Kirkwood, RN, Kiupel, M and Mulks, MH (2012). Defining the “core microbiome” of the microbial communities in the tonsils of healthy pigs. BMC Microbiology 12: 20.CrossRefGoogle ScholarPubMed
MacInnes, JI, Gottschalk, M, Lone, AG, Metcalf, DS, Ojha, SS, Rosendal, T, Watson, SB and Friendship, RM (2008). Prevalence of Actinobacillus pleuropneumoniae, Actinobacillus suis, Haemophilus parasuis, Pasteurella multocida, and Streptococcus suis in representative Ontario swine herds. Canadian Journal of Veterinary Research 72: 242248.Google ScholarPubMed
Makhanon, M, Tummaruk, P, Thongkamkoon, P, Thanawongnuwech, R and Prapasarakul, N (2012). Comparison of detection procedures of Mycoplasma hyopneumoniae, Mycoplasma hyosynoviae, and Mycoplasma hyorhinis in lungs, tonsils, and synovial fluid of slaughtered pigs and their distributions in Thailand. Tropical Animal Health and Production 44: 313318.Google Scholar
Marois, C, Le Carrou, J, Kobisch, M and Gautier-Bouchardon, AV (2007). Isolation of Mycoplasma hyopneumoniae from different sampling sites in experimentally infected and contact SPF piglets. Veterinary Microbiology 120: 96–104.CrossRefGoogle ScholarPubMed
Marois, C, Cariolet, R, Morvan, H and Kobisch, M (2008). Transmission of pathogenic respiratory bacteria to specific pathogen free pigs at slaughter. Veterinary Microbiology 129: 325332.Google Scholar
Moller, K, Andersen, LV, Christensen, G and Kilian, M (1993). Optimalization of the detection of NAD dependent Pasteurellaceae from the respiratory tract of slaughterhouse pigs. Veterinary Microbiology 36: 261271.CrossRefGoogle ScholarPubMed
Mulder, IE, Schmidt, B, Stokes, CR, Lewis, M, Bailey, M, Aminov, RI, Prosser, JI, Gill, BP, Pluske, JR, Mayer, CD, Musk, CC and Kelly, D (2009). Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology 7: 79.Google Scholar
Ngo, TH, Tran, TB, Tran, TT, Nguyen, VD, Campbell, J, Pham, HA, Huynh, HT, Nguyen, VV, Bryant, JE, Tran, TH, Farrar, J and Schultsz, C (2011). Slaughterhouse pigs are a major reservoir of Streptococcus suis serotype 2 capable of causing human infection in southern Vietnam. PloS One 6: e17943.Google Scholar
Opriessnig, T, Gimenez-Lirola, LG and Halbur, PG (2011). Polymicrobial respiratory disease in pigs. Animal Health Research Reviews/Conference of Research Workers in Animal Diseases 12: 133148.Google Scholar
Ortiz Martinez, P, Mylona, S, Drake, I, Fredriksson-Ahomaa, M, Korkeala, H and Corry, JE (2010). Wide variety of bioserotypes of enteropathogenic Yersinia in tonsils of English pigs at slaughter. International Journal of Food Microbiology 139: 6469.Google Scholar
O'Sullivan, T, Friendship, R, Blackwell, T, Pearl, D, McEwen, B, Carman, S, Slavic, D and Dewey, C (2011). Microbiological identification and analysis of swine tonsils collected from carcasses at slaughter. Canadian Journal of Veterinary Research 75: 106111.Google ScholarPubMed
Pennisi, E (2005). A mouthful of microbes. Science 307: 18991901.Google Scholar
Prakash, S, Tomaro-Duchesneau, C, Saha, S and Cantor, A (2011). The gut microbiota and human health with an emphasis on the use of microencapsulated bacterial cells. Journal of Biomedicine and Biotechnology 2011: 981214.Google Scholar
Pride, DT, Salzman, J, Haynes, M, Rohwer, F, Davis-Long, C, White, RA III, Loomer, P, Armitage, GC and Relman, DA (2011). Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME Journal 6: 915–26.CrossRefGoogle ScholarPubMed
Quince, C, Lanzen, A, Curtis, TP, Davenport, RJ, Hall, N, Head, IM, Read, LF and Sloan, WT (2009). Accurate determination of microbial diversity from 454 pyrosequencing data. Nature Methods 6: 639641.CrossRefGoogle ScholarPubMed
Quince, C, Lanzen, A, Davenport, RJ and Turnbaugh, PJ (2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38.CrossRefGoogle ScholarPubMed
Sallusto, F, Lanzavecchia, A and Mackay, C (1998). Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunology Today 19: 568574.Google Scholar
Santagati, M, Scillato, M, Patane, F, Aiello, C and Stefani, S (2012). Bacteriocin-producing oral streptococci and inhibition of respiratory pathogens. FEMS Immunology and Medical Microbiology 65: 2331.Google Scholar
Schutte, UM, Abdo, Z, Bent, SJ, Shyu, C, Williams, CJ, Pierson, JD and Forney, LJ (2008). Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Applied Microbiology and Biotechnology 80: 365380.Google Scholar
Shan, T, Li, L, Simmonds, P, Wang, C, Moeser, A and Delwart, E (2011). The fecal virome of pigs on a high-density farm. Journal of Virology 85: 1169711708.Google Scholar
Staats, JJ, Feder, I, Okwumabua, O and Chengappa, MM (1997). Streptococcus suis: past and present. Veterinary Research Communications 21: 381407.Google Scholar
Takahashi, T, Sunama, P, Satra, J, Cholsindhu, N, Kongthon, S, Jitnupong, W, Yamamoto, K, Kijima, M and Furuuchi, S (1999). Serotyping and pathogenicity of Erysipelothrix strains isolated from tonsils of slaughter pigs in Thailand. Journal of Veterinary Medical Science/The Japanese Society of Veterinary Science 61: 10071011.Google Scholar
Tonpitak, W, Rohde, J and Gerlach, GF (2007). Prevalence of “Actinobacillus porcitonsillarum” in porcine tonsils and development of a diagnosis duplex PCR differentiating between “Actinobacillus porcitonsillarum” and Actinobacillus pleuropneumoniae. Veterinary Microbiology 122: 157165.Google Scholar
Vouloumanou, EK, Makris, GC, Karageorgopoulos, DE and Falagas, ME (2009). Probiotics for the prevention of respiratory tract infections: a systematic review. International Journal of Antimicrobial Agents 34: 197.e1–197.10.CrossRefGoogle ScholarPubMed
Wohlgemuth, S, Loh, G and Blaut, M (2010). Recent developments and perspectives in the investigation of probiotic effects. International Journal of Medical Microbiology 300: 3–10.Google Scholar
Zhang, CP, Ning, YB, Zhang, ZQ, Song, L, Qiu, HS, Gao, HY and Fan, XZ (2009). Distributions of pathogenic capsular types and in vitro antimicrobial susceptibility of different serotypes of Streptococcus suis isolated from clinically healthy sows from 10 provinces in China. Zhonghua Liu Xing Bing Xue Za Zhi 30: 235238.Google Scholar
Zuckermann, FA (1999). Extrathymic CD4/CD8 double positive T cells. Veterinary Immunology and Immunopathology 72: 5566.Google Scholar