Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-05T14:02:46.899Z Has data issue: false hasContentIssue false
  • English
  • Français

Proliferative enteropathy: a global enteric disease of pigs caused by Lawsonia intracellularis

Published online by Cambridge University Press:  08 March 2007

Jeremy J. Kroll ,
Michael B. Roof ,
Lorraine J. Hoffman ,
James S. Dickson  and
D. L. Hank Harris
Jeremy J. Kroll*
Affiliation:
Department of Research and Development, Boehringer Ingelheim Vetmedica Inc., 2501 North Loop Drive, Ames, IA 50010, USA
Michael B. Roof
Affiliation:
Department of Research and Development, Boehringer Ingelheim Vetmedica Inc., 2501 North Loop Drive, Ames, IA 50010, USA
Lorraine J. Hoffman
Affiliation:
Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA
James S. Dickson
Affiliation:
Department of Animal Science, Iowa State University, Ames, IA 50011, USA
D. L. Hank Harris
Affiliation:
Department of Microbiology, Iowa State University, Ames, IA 50011, USA
*
*Corresponding author: Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Proliferative enteropathy (PE; ileitis) is a common intestinal disease affecting susceptible pigs raised under various management systems around the world. Major developments in the understanding of PE and its causative agent, Lawsonia intracellularis, have occurred that have led to advances in the detection of this disease and methods to control and prevent it. Diagnostic tools that have improved overall detection and early onset of PE in pigs include various serological and molecular-based assays. Histological tests such as immunohistochemistry continue to be the gold standard in confirming Lawsonia-specific lesions in pigs post mortem. Despite extreme difficulties in isolating L. intracellularis, innovations in the cultivation and the development of pure culture challenge models, have opened doors to better characterization of the pathogenesis of PE through in vivo and in vitro L. intracellularis–host interactions. Advancements in molecular research such as the genetic sequencing of the entire Lawsonia genome have provided ways to identify various immunogens, metabolic pathways and methods for understanding the epidemiology of this organism. The determinations of immunological responsiveness in pigs to virulent and attenuated isolates of L. intracellularis and identification of various immunogens have led to progress in vaccine development.

Keywords

PEileitisLawsonia intracellularis
Type
Research Article
Information
Animal Health Research Reviews , Volume 6 , Issue 2 , December 2005 , pp. 173 - 197
Copyright
Copyright © CAB International 2005

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

Al-Soud, WA and Radstrom, P (2001). Purification and characterization of PCR-inhibitory components in blood cells. Journal of Clinical Microbiology 39: 485–493.CrossRefGoogle ScholarPubMed
Alderton, M, Borland, R and Coloe, P (1992). Experimental reproduction of porcine proliferative enteritis. Journal of Comparative Pathology 106: 159–167.CrossRefGoogle ScholarPubMed
Bakker, J, van der Heijden, HMJF, De Smet, M and Vos, J (2000). Comparison of laboratory techniques for the diagnosis of porcine proliferative enteropathy (PPE) in fattening pigs. In: Proceedings in the 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 25.Google Scholar
Barna, P and Bilkei, G (2003). Effect of gilt seropositivity to Lawsonia intracellularis (LI) on their offspring's seropositivity to LI, and on diarrhoea after a pure-culture challenge. Preventative Veterinary Medicine 61: 71–78.Google Scholar
Beckler, DC, Mahlum-Wees, C, Guedes, RMC and Gebhart, CJ (2003). Development and comparison of tests for detecting faecal shedding of Lawsonia intracellularis. In: Proceedings of the American Association of Swine Veterinarians, Des Moines, IA, USA, pp. 81–82.Google Scholar
Beckler, DC, Kapur, V and Gebhart, CJ (2004). Molecular epidemiologic typing of Lawsonia intracellularis. In: Conference for Research Workers in Animal Diseases, Gastroenteric Diseases section, Abstract 106, pp. 124.Google Scholar
Beister, H and Schwarte, L (1931). Intestinal adenoma in swine. American Journal of Pathology 7: 175–185.Google Scholar
Bilkei, G (1996). The management of veterinary extension activities and the practical experiences of pig breeding advisory bureaus in Western Europe. In: Proceedings of the Pig Days, University of Budapest, Hungary, pp. 1–3.Google Scholar
Boesen, HT, Jensen, TK, Schmidt, AS, Jensen, BB, Jensen, SM and Moller, K (2004). The influence of diet on Lawsonia intracellularis colonization in pigs upon experimental challenge. Veterinary Microbiology 103: 35–45.CrossRefGoogle ScholarPubMed
Boesen, HT, Jensen, TK, Jungersen, G, Riber, U, Boye, M and Moller, K (2005a). Development, characterization and diagnostic application of a monoclonal antibody specific for a proteinase K resistant Lawsonia intracellularis antigen. Veterinary Microbiology 105: 199–206.Google Scholar
Boesen, HT, Jensen, TK, Moller, K, Nielsen, LH and Jungersen, G (2005b). Evaluation of a novel enzyme-linked immunosorbent assay for serological diagnosis of porcine proliferative enteropathy. Veterinary Microbiology 109: 105–112.Google Scholar
Boosinger, T, Thacker, H and Armstrong, C (1985). Campylobacter sputorum subsp. Mucosalis and Campylobacter hyointestinalis infections in the intestine of gnotobiotic pigs. American Journal of Veterinary Research 46: 2152–2156.Google ScholarPubMed
Bronsvoort, M, Norby, B, Bane, D and Gardner, I (2001). Management factors associated with seropositivity to Lawsonia intracellularis in US swine herds. Journal of Swine Health and Production 9: 285–290.Google Scholar
Chalmers, G, Nation, P and Pritchard, J (1990). Terminal ileitis in lambs. Canadian Veterinarian Journal 31: 292–295.Google ScholarPubMed
Chang, WL, Wu, CF, Wu, Y, Kao, YM and Pan, MJ (1997). Prevalence of Lawsonia intracellularis in swine herds in Taiwan. Veterinary Record 141: 103–104.CrossRefGoogle ScholarPubMed
Chouet, S, Prieto, C, Mieli, L, Veenhuizen, M and McOrist, S (2003). Patterns of exposure to Lawsonia intracellularis infection on European pig farms. Veterinary Record 152: 14–17.CrossRefGoogle ScholarPubMed
Collins, J, Libal, M and Brost, D (1983). Proliferative enteritis in two pups. Journal of American Veterinary Medical Association 183: 886–889.Google Scholar
Collins, AM, Swift, I and Monckton, RP (1996). Replication of Australian porcine isolates of Ileal symbiont intracellularis in tissue culture. Veterinary Microbiology 49: 249–255.CrossRefGoogle ScholarPubMed
Collins, A, Love, R, Pozo, J, Smith, S and McOrist, S (2000). Studies on ex vivo survival of Lawsonia intracellularis. Swine Health and Production 8: 211–215.Google Scholar
Collins, AM, van Dijk, M, Vu, NQ, Pozo, J and Love, RJ (2001). Immunity to Lawsonia intracellularis. In: Proceedings of the Allen D. Leman Swine Conference, Minneapolis, MN, USA, pp. 115–120.Google Scholar
Cooper, DM (1996). Proliferative enteritis in the hamster, horse, deer and ostrich: detection and characterization of Lawsonia intracellularis. MS Thesis, University of Minnesota, Minneapolis-St. Paul, MN, USA.Google Scholar
Cooper, D, Swanson, D and Gebhart, CJ (1997). Diagnosis of proliferative enteritis in frozen and formalin-fixed, paraffin-embedded tissues from a hamster, horse, deer and ostrich using a Lawsonia -specific multiplex PCR assay. Veterinary Microbiology 54: 47–62.CrossRefGoogle ScholarPubMed
Corzo, CA, Friendship, R, Dewey, C and Blackwell, T (2005). Comparison of 2 serologic tests for the diagnosis of porcine proliferative enteropathy. Canadian Veterinary Journal 46: 433–435.Google Scholar
Cutler, R and Gardner, I (1989). A blueprint for pig health research. Australian Pig Research Council Publication. Canberra, Australia: Australian Research Council.Google Scholar
Dale, CJ, Moses, EK, Ong, CC, Morrow, CJ, Reed, MB, Hasse, D and Strugnell, RA (1998). Identification and sequencing of the groE operon and flanking genes of Lawsonia intracellularis: use in phylogeny. Microbiology 144: 2073–2084.Google Scholar
Drolet, R, Larochelle, D and Gebhart, CJ (1996). Proliferative enteritis associated with Lawsonia intracellularis (Ileal Symbiont intracellularis) in white-tailed deer. Journal of Veterinary Diagnostic Investigation 8: 250–253.CrossRefGoogle ScholarPubMed
Dunser, M, Untersperger, M, Schweighardt, H and Schuh, M (2000). Comparative studies by PCR, and indirect immunoflourescent antibody test on the occurence of Lawsonia intracellularis in upper Austrian swine herds. In: Proceedings in the 16th International Pig Veterinary Society Congress, Melbourne, Australia, p. 59.Google Scholar
Elder, RO, Duhamel, GE, Mathiesen, MR, Erickson, ED, Gebhart, CJ and Oberst, RD (1997). Multiplex polymerase chain reaction for simultaneous detection of Lawsonia intracellularis, Serpulina hyodysenteriae, and salmonellae in porcine intestinal specimens. Journal of Veterinary Diagnostic Investigation 9: 281–286.Google Scholar
Elwell, M, Chapman, A and Frenkel, J (1981). Duodenal hyperplasia in a guinea pig. Veterinary Pathology 18: 136–139.CrossRefGoogle Scholar
Eriksen, K and Landsverk, T (1985). Intestinal adenomatosis in the blue fox. Nordic Veterinary Medicine 37: 254–255.Google Scholar
Erikson, K, Landsverk, T and Bratberg, B (1990). Morphology and immunoperoxidase studies of intestinal adenomatosis in the blue fox, Alopex lagopus. Journal of Comparative Pathology 102: 265–278.CrossRefGoogle Scholar
Ewing, EP, Takeuchi, JA, Shirai, A and Osterman, JV (1978). Experimental infection of mouse peritoneal mesothelium with scrub typhus rickettsia: an ultrastructural study. Infection and Immunity 19: 1068–1075.Google Scholar
Fourchon, P and Chouet, S (2000). Technical results of swine herds and serological results on pigs for Lawsonia intracellularis. In: Proceedings of the 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 62.Google Scholar
Fox, A and Lawson, GHK (1988). Campylobacter-like omega intracellular antigen in proliferative colitis of ferrets. Lab Animal Science 38: 34–36.Google Scholar
Fox, JG, Dewhirst, FE, Fraser, GJ, Paster, BJ, Shames, B and Murphy, JC (1994). Intracellular Campylobacter-like organism from ferrets and hamsters with proliferative bowel disease is a Desulfovibrio sp. Journal of Clinical Microbiology 32: 1229–1237.CrossRefGoogle ScholarPubMed
Frisk, C and Wagner, J (1977). Experimental hamster enteritis: an electron microscopic study. American Journal of Veterinary Research 38: 1861–1868.Google ScholarPubMed
Gaillard, J, Berche, LP, Moounier, J, Richard, S and Sansonetti, P (1987). In vitro model of penetration and intracellular growth of Listeria monocytogenes in human enterocyte-like cell line CaCo-2. Infection and Immunity 55: 2822–2829.Google Scholar
Gebhart, C and Guedes, R (2001). Proliferative enteropathy: diagnosis and immunity. In: Proceedings of the American Association of Swine Veterinarians, Nashville, TN, USA, 24–27 February, pp. 353–358Google Scholar
Gebhart, C and Kapur, V (2003). The complete genomic sequence of Lawsonia intracellularis University of Minnesota, Minneapolis-St. Paul, MN, USA. Available at http://patho- genomics.ahc.umn.edu/lawsonia_index.htmGoogle Scholar
Gebhart, C, Ward, G, Chang, K and Kurtz, H (1983). Campylobacter hyointestinalis (new species) isolate from swine with lesions of proliferative enteritis. American Journal of Veterinary Research 44: 361–367.Google Scholar
Gebhart, CJ, Lin, GF, McOrist, S, Lawson, GHK and Murtaugh, MP (1991). Cloned DNA probes specific for the intracellular Campylobacter-like organism of porcine proliferative enteritis. Journal of Clinical Microbiology 29: 1011–1015.CrossRefGoogle ScholarPubMed
Gebhart, C, Barns, S, McOrist, S, Lin, G and Lawson, G (1993). Ileal symbiont intracellularis, an obligate intracellular bacterium of porcine intestines showing a relationship to Desulfovibrio species. International Journal of Systematic Bacteriology 43: 533–538.Google Scholar
Guedes, RMC (2004). Update on epidemiology and diagnosis of porcine proliferative enteropathy. Journal Swine Health and Production 12: 134–138.Google Scholar
Guedes, RMC and Gebhart, CJ (2002c). Comparison of challenge models for porcine proliferative enteropathy. In: Proceedings of the 17th International Pig Veterinary Society Congress, Ames, IA, USA, pp. 49.Google Scholar
Guedes, RMC and Gebhart, CJ (2003a). Onset and duration of faecal shedding, cell-mediated and humoral immune responses in pigs after challenge with a pathogenic isolate or an attenuated vaccine strain of Lawsonia intracellularis. Veterinary Microbiology 91: 135–145.Google Scholar
Guedes, RMC and Gebhart, CJ (2003b). Comparison of the intestinal mucosa homogenate and pure culture of the homologous Lawsonia intracellularis isolate in reproducing proliferative enteropathy in swine. Veterinary Microbiology 93: 159–166.Google Scholar
Guedes, RMC and Gebhart, CJ (2003c). Preparation and characterization of polyclonal and monoclonal antibodies against Lawsonia intracellularis. Journal of Veterinarian Diagnostic Investigation 15: 438–446.Google Scholar
Guedes, RMC, Gebhart, CJ, Deen, J and Winkelman, N (2002a). Validation of an immunoperoxidase monolayer assay as a serologic test for porcine proliferative enteropathy. Journal of Veterinary Diagnostic Investigation 14: 528–530.Google Scholar
Guedes, RMC, Gebhart, CJ, Winkelman, NL, Mackie-Nuss, RAC, Marsteller, TA and Deen, J (2002b). Comparison of different methods for diagnosis of porcine proliferative enteropathy. Canadian Journal of Veterinary Research 66: 99–107.Google ScholarPubMed
Guedes, RMC, Winkelman, NL and Gebhart, CJ (2003a). Relationship between the severity of porcine proliferative enteropathy and the infectious dose of Lawsonia intracellularis. Veterinary Record 153: 432–433.CrossRefGoogle ScholarPubMed
Guedes, RMC, Gebhart, CJ, Winkelman, NL and Mackie-Nuss, RA (2003b). A comparative study of an indirect fluorescent antibody test and an immunoperoxidase monolayer assay for the diagnosis of porcine proliferative enteropathy. Journal of Veterinary Diagnostic Investigation 14: 420–423.Google Scholar
Haugegaard, J, Szancer, J, Hansen, KK, Ripley, P and Fisch, R (2000). Evaluation of the efficacy of ECONOR (valnemulin) in the treatment of a naturally occurring outbreak of porcine proliferative enteropathy (PPE) (ileitis) in Denmark. In: Proceedings of the 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 76.Google Scholar
HolyoakePK (1993). Epidemiology of proliferative enteritis in pigs. PhD Thesis, University of Melbourne, Melbourne, Australia.Google Scholar
Holyoake, PK, Cutler, RS, Caple, IW and Monckton, RP (1994). Enzyme-linked immunosorbent assay for measuring Ileal Symbiont intracellularis-specific immunoglobulin G response in sera of pigs. Journal of Clinical Microbiology 32: 1980–1985.Google Scholar
Huerta, B, Arenas, A, Carrasco, L, Maldonaldo, A, Tarradas, C, Carbonero, A and Perea, A (2003). Comparison of diagnostic techniques for porcine proliferative enteropathy (Lawsonia intracellularis infection). Journal of Comparative Pathology 129: 179–185.Google Scholar
Jacobson, M, Englund, S and Ballagi-Pordany, A (2003a). The use of a mimic to detect polymerase chain reaction-inhibitory factors in faeces examined for the presence of Lawsonia intracellularis. Journal of Veterinary Diagnostic Investigation 15: 268–273.Google Scholar
Jacobson, M, Hard af Segertad, C, Gunnasrsson, A, Fellstrom, C, de Verdier Klingenberg, K, Wallgren, P and Jensen-Waern, M (2003b). Diarrhoea in the growing pig–a comparison of clinical, morphological and microbial findings between animals from good and poor performance herds. Research in Veterinary Science 74: 163–169.Google Scholar
Jacobson, M, Aspan, A, Heldtander Konigsson, M, Hard af Segerstad, C, Wallgren, P, Fellstrom, C, Jensen-Waern, M and Gunnarson, A. (2004). Routine diagnostics of Lawsonia intracellularis performed by PCR, serological and post mortem examination, with special emphasis on sample preparation methods for PCR. Veterinary Microbiology 102: 189–201.CrossRefGoogle ScholarPubMed
Jacoby, RO (1978). Transmissible ileal hyperplasia of hamsters. American Journal of Pathology 91: 433–444.Google ScholarPubMed
Jansi, S, McOrist, S and Lawson, GHK (1994). Experimentally induced proliferation enteritis in hamsters: an ultrastructural study. Research in Veterinary Science 56: 186–192.Google Scholar
Jensen, TK and Svensmark, B (2000). Unusual detection site of Lawsonia intracellularis: in cases of peritonitis and in the liver. In: Proceedings of the 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 64.Google Scholar
Jensen, TK, Moller, K, Leser, TD and Jorsal, SE (1997). Comparison of histology, immunohistochemistry and polymerase chain reaction for detection of Lawsonia intracellularis in natural porcine proliferative enteropathy. European Journal of Veterinary Pathology 3: 115–123.Google Scholar
Jensen, TK, Moller, K, Lindecrona, R and Jorsal, SE (2000). Detection of Lawsonia intracellularis in the tonsils of pigs with proliferative enteropathy. Research in Veterinary Science 68: 23–26.Google Scholar
Joens, LA, Nibbelink, D and Glock, RD (1997). Induction of gross and microscopic lesions of porcine proliferative enteritis by Lawsonia intracellularis. American Journal of Veterinary Research 58: 1125–1131.Google Scholar
Jones, G, Ward, G, Murtaugh, M, Lin, G and Gebhart, CJ (1993a). Enhanced detection of intracellular organism of swine proliferative enteritis, ileal symbiont intracellularis, in faeces by polymerase chain reaction. Journal of Clinical Microbiology 31: 2611–2615.CrossRefGoogle ScholarPubMed
Jones, G, Davies, PR, Rose, R, Ward, GE and Murtaugh, MP (1993b). Comparison of techniques for diagnosis of proliferative enteritis of swine. American Journal of Veterinary Research 54: 1980–1985.Google Scholar
Jones, GF, Ward, GE, Murtaugh, MP, Rose, R and Gebhart, CJ (1993c). Relationship between Ileal Symbiont Intracellularis and porcine proliferative enteritis. Infection and Immunity 61: 5237–5244.CrossRefGoogle ScholarPubMed
Jones, GF, Ward, GE, Gebhart, CJ, Murtaugh, MP and Collins, JE (1993d). Use of a DNA probe to detect the intracellular organism of proliferative enteritis in swine faeces. American Journal of Veterinary Research 54: 1585–1590.Google Scholar
Jordan, DM, Knittel, JP, Roof, MB, Schwartz, KJ, Larson, DJ and Hoffman, LJ (1999). Detection of Lawsonia intracellularis in Iowa swine using polymerase chain reaction methodology. Journal of Veterinary Diagnostic Investigation 11: 45–49.Google Scholar
Jordan, DJ, Knittel, JP, Schwartz, KJ, Roof, MB and Hoffman, LJ (2004). A Lawsonia intracellularis transmission study using a pure culture inoculated seeder-pig sentinel model. Veterinary Microbiology 104: 83–90.CrossRefGoogle ScholarPubMed
Just, SD, Thoen, CO, Thacker, BJ and Thompson, JU (2001). Monitoring of Lawsonia intracellularis by indirect serum immunofluorescence assay in a commercial swine production system. Journal of Swine Health and Production 9: 57–61.Google Scholar
Kashiwazaki, M, Namioka, S and Yabiki, T (1971). Gnotobiotic pigs exposed to Vibrio coli. National Institute of Animal Health Quarterly 11: 145–150.Google ScholarPubMed
Keita, A, Westhoff, D, Pagot, E, Orveillion, FX and Pommier, P (2004). Field study into safety of Enterisol® Ileitis on a Lawsonia intracellularis positive French farm. In: Proceedings of the 18th International Pig Veterinary Society Congress, Hamburg, Germany, pp. 273. Proliferative enteropathy 193Google Scholar
Klein, E, Gebhart, CJ and Duhamel, G (1999). Fatal outbreaks of proliferative enteritis caused by Lawsonia intracellularis in young colony-raised rhesus macaques. Journal of Medical Primatology 28: 11–18.Google Scholar
Knittel, J (1999). Porcine proliferative enteropathy and Lawsonia intracellularis. Compendium on Continuing Education for the Practicing Veterinarian 21: S53–S77.Google Scholar
Knittel, JP and Roof, MB (1998). United States patent for cultivation of ileal symbiont intracellularis propagation in suspended host cells. United States Patent No. 5, 714, 375.Google Scholar
Knittel, JP and Roof, MB (1999). United States patent for Lawsonia intracellularis cultivation, anti- Lawsonia intracellularis vaccines and diagnostic agents. United States Patent No. 8, 885, 823.Google Scholar
Knittel, JP, Larson, DI, Harris, DL, Roof, MB and McOrist, S (1996). United States isolates of Lawsonia intracellularis from porcine proliferative enteropathy resemble European isolates. Swine Health and Production 4: 119–122.Google Scholar
Knittel, JP, Roof, MB, Schwartz, KJ, McOrist, S and Harris, DL (1997). Diagnosis of porcine proliferative enteritis. Compendium on Continuing Education for the Practicing Veterinarian 19: S26–S29.Google Scholar
Knittel, JP, Jordan, DJ, Schwartz, KJ, Janke, B, Roof, MB, McOrist, S and Harris, DL (1998). Evaluation of antemortem polymerase chain reaction and serological methods for detection of Lawsonia intracellularis-exposed pigs. American Journal of Veterinary Research 59: 722–726.Google Scholar
Ko, J and Splitter, GA (2003). Molecular host-pathogen interaction in brucellosis: current understanding and future approaches to vaccine development for mice and humans. Clinical Microbiology Reviews 16: 65–78.Google Scholar
Kolb, J, Sick, F and Walter, D (2004). Efficacy of an avirulent live Lawsonia intracellularis vaccine in pigs. In: Proceedings of the 18th International Pig Veterinary Society Congress, Hamburg, Germany, pp. 437.Google Scholar
Koyama, T, Hiria, T and Nagai, S (2004). In vitro cultivation and partial characterization of Lawsonia intracellularis from a Japanese field case of porcine proliferative enteropathy. In: Proceedings from the 18th International Pig Veterinary Society Congress, Hamburg, Germany, pp. 307.Google Scholar
Kroll, JJ, Roof, MB and McOrist, S (2004a). Evaluation of protective immunity in pigs following oral administration of an avirulent live vaccine of Lawsonia intracellularis. American Journal of Veterinary Research 65: 559–565.Google Scholar
Kroll, J, Roof, M, Elbers, K, Walter, D and Utley, P (2004b). Enterisoll Ileitis: induction of immunity to control ileitis in swine. In: Proceedings of the 18th International Pig Veterinary Society Congress, Hamburg, Germany, pp. 832.Google Scholar
Kroll, JJ, Roof, MB and McOrist, S (2005a). Maternal antibody exposure and vaccination with an oral avirulent live Lawsonia intracellularis vaccine (Enterisol Ileitis) in pigs. Research in Veterinary Science, submitted, May 2005.Google Scholar
Kroll, JJ, Eichmeyer, MA, Schaeffer, ML, McOrist, S, Harris, DL and Roof, MB (2005b). Lipopolysaccaride-based enzyme-linked immunosorbent assay for experimental use in detection of antibodies to Lawsonia intracellularis in pigs. Clinical and Diagnostic Laboratory Immunology 12: 693–699.Google Scholar
Kyriakis, SC, Bourtzi-Hatzopoulou, E, Alexopoulos, C, Kritas, SK, Polyzopoulou, Z, Lekkas, S and Gardey, L (2002a). Field evaluation of the effect of in-feed doxycycline for the control of ileitis in weaned pigs. Journal of Veterinary Medicine, Series B 49: 317–324.Google Scholar
Kyriakis, SC, Alexopoulos, C, Saoulidis, K, Lekkas, S, Miliotis, CCH and Sauveroche, B (2002b). The effect of josamycine on the control of ileitis in weaned piglets under field conditions. Journal of Veterinary Pharmacology and Therapy 25: 279–284.Google Scholar
La, T, Collins, AM, Phillips, ND, Oksa, A and Hampson, DJ (2004). Evaluation of a multiplex-PCR for the detection of Brachyspira hyodysenteriae, Brachyspira pilosicoli and Lawsonia intracellularis in pig faeces. In: Proceedings of the 18th IPVS Congress, Hamburg, Germany, pp. 283.Google Scholar
Lantz, PG, Al-Soud, WA, Knutsson Hahn-Hagerdal, B and Radstrom, P (2000). Biotechnical use of polymerase chain reaction for microbiological analysis of biological samples. Biotechnology Annual Reviews 5: 87–130.Google Scholar
Lawson, GHK and Gebhart, CJ (2000). Proliferative enteropathy. Journal of Comparative Pathology 122: 77–100.Google Scholar
Lawson, GHK, Rowland, AC, Roberts, I, Fraser, G and McCartney, E (1979). Proliferative haemorrhagic enteropathy. Research in Veterinary Science 27: 46–51.CrossRefGoogle ScholarPubMed
Lawson, G, Rowland, A and MacIntyre, N (1985). Demonstration of a new intracellular antigen in porcine intestinal adenomatosis and hamster proliferative enteritis. Veterinary Microbiology 10: 303–313.Google Scholar
Lawson, GHK, McOrist, S, Rowland, AC, McCartney, E and Roberts, L (1988). Serological diagnosis of the porcine proliferative enteropathies: implications for aetiology and epidemiology. Veterinary Record 122: 554–557.Google Scholar
Lawson, G, McOrist, S, Jansi, S and Mackie, R (1993). Intracellular bacteria of porcine proliferative enteropathy: cultivation and maintenance in vitro. Journal of Clinical Microbiology 31: 1136–1142.Google Scholar
Lawson, GHK, Mackie, RAM, Smith, DGE and McOrist, S (1995). Infection of cultured rat enterocytes by ileal symbiont intracellularis depends on host cell function and actin polymerization. Veterinary Microbiology 45: 339–350.Google Scholar
LeMarchand, T, Duncan, D, Tully, J and Lopez, M (1995). Intracellular Campylobacter-like organisms associated with cloacal prolapse and enterocolitis in emus (Dromaiu novaehollandiae) Veterinary Pathology 32: 587Google Scholar
Lindecrona, RH, Jensen, TK, Andersen, PH and Moller, K (2002). Application of a 5' nuclease assay for detection of Lawsonia intracellularis in faecal samples from pigs. Journal of Clinical Microbiology 40: 984–987.Google Scholar
Lofstedt, M, Holmgren, N, Jacobsen, M, Fellstrom, C and Lundeheim, N (2004). Lawsonia intracellularis and Brachyspira species in Swedish growers. In: Proceedings of the 18th IPVS Congress, Hamburg, Germany, pp. 289.Google Scholar
Lomax, G, Glock, R, Harris, DL and Hogan, J (1982a). Porcine proliferative enteritis: experimentally induced disease in cesarean-derived colostrum-deprived pigs. American Journal of Veterinary Research 43: 1622–1630.Google Scholar
Lomax, G, Glock, R and Hogan, J (1982b). Experimentally induced proliferative enteritis in specific-pathogen-free pigs. American Journal of Veterinary Research 43: 1615–1620.Google ScholarPubMed
Love, DN and Love, RJ (1979). Pathology of proliferative haemorrhagic enteropathy in pigs. Veterinary Pathology 16: 41–48.Google Scholar
Love, D, Love, R and Bailey, M (1977). Comparison of Campylobacter sputorum subspecies mucosalis strains in PIA, and PHE Veterinary Record 101: 473Google Scholar
MacIntyre, N, Smith, DG, Shaw, DJ, Thomson, JR and Rhind, SM (2003). Immunopathogenesis of experimentally induced proliferative enteropathy in pigs. Veterinary Pathology 40: 421–432.CrossRefGoogle ScholarPubMed
Mapother, ME, Joens, LA and Glock, RD (1987). Experimental reproduction of porcine proliferative enteritis. Veterinary Record 121: 533–536.Google Scholar
Marsteller, TA, Winkelman, NL, Gebhart, CJ, Armbruster, GA, Weldon, WMR, Weatherford, J and Symanowski, J (2000). Efficacy of Tylan 200 injection for the treatment and control of porcine proliferative enteropathy caused by Lawsonia intracellularis in swine. In: Proceedings of the American Association of Swine Practitioners, pp. 233–238.Google Scholar
Marsteller, TA, Armbruster, G, Bane, DP, Gebhart, CJ, Muller, R, Weatherford, J and Thacker, B (2003). Monitoring the prevalence of Lawsonia intracellularis IgG antibodies using serial sampling in growing breeding swine herds. Journal of Swine Health and Production 11: 127–130.Google Scholar
Mauch, CHY and Bilkei, G (2004). Effect of sow parity on the transmission of Lawsonia intracellulari s to piglets Veterinary Record 155: 532Google Scholar
McCartney, E, Lawson, GHK and Rowland, A (1984). Behaviour of Campylobacter sputorium sub-species mucosalis in gnotobiotic pigs. Research in Veterinary Science 36: 290–297.Google Scholar
McCluskey, J, Hannigan, J, Harris, J, Wren, B and Smith, DGE (2002). LsaA, an antigen involved in cell attachment and invasion, is expressed by Lawsonia intracellularis during infection in vitro and in vivo. Infection and Immunity 70: 2899–2907.CrossRefGoogle ScholarPubMed
McOrist, S (2005). Defining the full costs of endemic porcine proliferative enteropathy. The Veterinary Journal 170: 8–9.CrossRefGoogle ScholarPubMed
McOrist, S and Gebhart, CJ (1995). In vitro testing of antimicrobial agents for proliferative enteropathy (ileitis). Swine Health and Production 3: 146–149.Google Scholar
McOrist, S and Gebhart, CJ (1999). Porcine proliferative entero- pathies. In: Straw, B, Mengeling, W, D'Allaire, S and Taylor, D (eds) Diseases of Swine, 8th edn. Ames, IA, USA: Iowa State University Press, pp. 521–534.Google Scholar
McOrist, S and Lawson, GHK (1989). Proliferative enteropathies: Campylobacter species in the faeces of normal and contact pigs Veterinary Record 124: 124Google Scholar
McOrist, S, Boid, R, Lawson, GHK and McConnell, I (1987). Monoclonal antibodies to intracellular campylobacter-like organisms of the porcine proliferative enteropathies. Veterinary Record 121: 421–422.Google Scholar
McOrist, S, MacIntyre, N, Stokes, CR and Lawson, GHK (1992). Immunocytological responses in porcine proliferative enteropathies. Infection and Immunity 60: 4184–4191.Google Scholar
McOrist, S, Jansi, S, Mackie, R, MacIntyre, N, Neef, N and Lawson, GHK (1993). Reproduction of porcine proliferative enteropathy with pure culture isolates of ileal symbiont intracellularis. Infection and Immunity 61: 4286–4292.Google Scholar
McOrist, S, Mackie, R, Neef, N, Aitken, L and Lawson, GHK (1994a). Synergism of ileal symbiont intracellularis and gut bacteria in the reproduction of porcine proliferative enteropathy. Veterinary Record 134: 331–332.Google Scholar
McOrist, S, Gebhart, CJ and Lawson, GHK (1994b). Polymerase chain reaction for the diagnosis of porcine proliferative enteropathy. Veterinary Microbiology 41: 201–212.Google Scholar
McOrist, S, Gebhart, C, Boid, R and Barns, S (1995a). Characterization of Lawsonia intracellularis gen. nov., sp. nov., the obligately intracellular bacterium of porcine proliferative enteropathy. International Journal of Systematic Bacteriology 45: 820–825.Google Scholar
McOrist, S, Mackie, RA and Lawson, GHK (1995b). Antimicrobial susceptibility of ileal symbiont intracellularis isolated from pigs with proliferative enteropathy. Journal of Clinical Microbiology 33: 1314–1317.Google Scholar
McOrist, S, Jasni, S, Mackie, RA, Berschneider, HM, Rowland, AC and Lawson, GHK (1995c). Entry of the bacterium ileal symbiont intracellularis into cultured enterocytes and its subsequent release. Research in Veterinary Science 59: 255–260.Google Scholar
McOrist, S, Roberts, L, Jasni, S, Rowland, AC, Lawson, GHK, Gebhart, CJ and Bosworth, B (1996a). Developed and resolving lesions in porcine proliferative enteropathy: possible pathogenic mechanisms. Journal of Comparative Pathology 115: 35–45.Google Scholar
McOrist, S, Smith, SH, Shearn, FH, Carr, MM and Miller, DJS (1996b). Treatment and prevention of porcine proliferative enteropathy with oral tiamulin. Veterinary Record 139: 615–618.Google Scholar
McOrist, S, Smith, SH and Green, LE (1997a). Estimate of direct financial losses due to porcine proliferative enteropathy. Veterinary Record 140: 579–581.Google Scholar
McOrist, S, Morgan, J, Veenhuizen, MF, Lawrence, K and Kroger, HW (1997b). Oral administration of Tylosin phosphate for treatment and prevention of proliferative enteropathy in pigs. American Journal of Veterinary Research 58: 136–139.CrossRefGoogle ScholarPubMed
McOrist, S, Mackie, RAM, Lawson, GHK and Smith, DGE (1997c). In-vitro interactions of Lawsonia intracellularis with cultured enterocytes. Veterinary Microbiology 54: 385–392.Google Scholar
McOrist, S, Shearn, MF and Morgan, J (1999). Control of porcine proliferative enteropathy by oral administration of chlortetracycline. Veterinary Record 144: 48–49.Google Scholar
McOrist, S, Muller Wager, A, Kratzer, D and Sjosten, CG (2000). Therapeutic efficacy of water-soluble lincomycin-spectinomycin powder against porcine proliferation enteropathy in a European field study. Veterinary Record 146: 61–65.Google Scholar
McOrist, S, Barcellos, D and Wilson, R (2003). Global patterns of porcine proliferative enteropathy. The Pig Journal 51: 26–35.Google Scholar
Moller, K, Jensen, TK and Jorsal, SE (1998a). Detection of Lawsonia intracellularis in endemically infected pig herds. In: Proceedings of the 15th International Pig Veterinary Society, Birmingham, UK, pp. 63.Google Scholar
Moller, K, Jensen, TK, Jorsal, SE, Leser, TD and Carstensen, B (1998b). Detection of Lawsonia intracellularis, Serpulina hyodysenteriae, weakly beta-haemolytic intestinal spirochaetes, Salmonella enterica, and haemolytic Escherichia coli from swine herds with and without diarrhoea among growing pigs. Veterinary Microbiology 62: 59–72.Google Scholar
Morrison, RP and Caldwell, HD (2002). Immunity to murine chlamydial genital infection. Infection and Immunity 70: 2741–2751.Google Scholar
Mortimer, I, Van der Heijden, HMJF, Henderson, LE, Thomson, JR and Lawrence, K (2000). Proficiency testing among European laboratories using an immuno-fluorescent antibody test (IFAT) for the detection of antibodies against Lawsonia intracellularis in pigs. In: Proceedings of the 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 77.Google Scholar
Nuntaprasert, A, Kaur, K, Gebhart, CJ and Kapur, V (2004). Expression and purification of a flagellar protein of Lawsonia intracellularis. In: Proceedings of the Conference of Research Workers in Animal Diseases, Chicago, IL, USA, pp. 124.Google Scholar
Plawinska, J, Jakubowski, T, Rzewuska, M and Binek, M (2004). Occurrence of Lawsonia intracellularis and Brachyspira spp. infection in swine suffering from diarrhoea. In: Proceedings of the 18th IPVS Congress, Hamburg, Germany, pp. 287.Google Scholar
Reynolds, DJ and Pearce, JH (1991). Endocytic mechanisms utilized by Chlamydiae and their influence on introduction of productive infection. Infection and Immunity 59: 3033–3039.Google Scholar
Roberts, L, Rowland, A and Lawson, G (1977). Experimental reproduction of porcine intestinal adenomatosis and necrotic enteritis. Veterinary Record 100: 12–13.Google Scholar
Roberts, L, Roland, A and Lawson, GHK (1980). Porcine intestinal adenomatosis: epithelial dysplasia and infiltration. Gut 21: 1035–1040.CrossRefGoogle ScholarPubMed
Roitt, I, Bronstoff, J and Male, D (1998). Hypersensitivity – Type IV. In: Crowe, L (ed.) Immunology, 5th edn. St Louis, USA: Mosby International Ltd, pp. 341–352.Google Scholar
Rowland, A and Lawson, GHK (1974). Intestinal adenomatosis in the pig: immunoflourescent and electron microscopic studies. Research in Veterinary Science 17: 323–330.Google Scholar
Rowland, A and Lawson, GHK (1992). Porcine proliferative enteropathies. In: Straw, B, Mengeling, W, D'Allaire, S and Taylor, D (eds) Diseases of Swine, 7th edn. Ames, IA, USA: Iowa State University Press, pp. 560–569.Google Scholar
Rowland, A, Lawson, GHK and Maxwell, A (1973). Intestinal adenomatosis in the pig: occurrence of a bacterium in affected cells Nature 247: 247Google Scholar
Rowland, AC (1978). Necrotic enteritis and regional ileitis in pigs at slaughter. Veterinary Record 100: 338–339.CrossRefGoogle Scholar
Rowland, AC and Rowntree, PGM (1972). A haemorrhagic bowel syndrome associated with intestinal adenomatosis in the pig. Veterinary Record 91: 235–241.Google Scholar
Sansonetti, PJ (1992). Molecular and cellular biology of Shigella flexneri invasiveness: from cell assay systems to shigellosis. Current Topics in Microbiology and Immunology 180: 1–19.Google Scholar
Sapico, F, Reeves, D, Wexler, H, Duncan, J, Wilson, K and Finegold, S (1994). Preliminary study using species-specific oligonucleotide probe for rRNA of Bilophila wadsworthia. Journal of Clinical Microbiology 32: 2510–2513.Google Scholar
Schwartz, K, Knittel, J, Walter, D, Roof, M and Anderson, M (1999). Effect of oral tiamulin on the development of porcine proliferative enteropathy in a pure-culture challenge model. Swine Health and Production 7: 5–11.Google Scholar
Shaw, J, Grund, V, Durling, L, Crane, D and Caldwell, HD (2002). Dendritic cells pulsed with a recombinant chlamydial major outer membrane protein antigen elicit a CD4+ type 2 rather than type 1 immune response that is not protective. Infection and Immunity 70: 1097–1105.Google Scholar
Shultz, RA, McOrist, S and Shearn, M (1997). Titration of a BMD/CTC combination for control of Porcine Proliferative Enteropathy. In: Proceedings of the American Association of Swine Practitioners, Quebec, Canada, pp. 109–111.Google Scholar
Sick, F, Hayes, P and Kolb, J (2002). Enterisol Ileitis vaccine; field efficacy evaluation. In: Proceedings of the American Association of Swine Veterinarians, Kansas City, Missouri, pp. 161–163.Google Scholar
Smith, SH and McOrist, S (1997). Development of persistent intestinal infection and excretion of Lawsonia intracellularis by piglets. Research in Veterinary Science 62: 6–10.Google Scholar
Smith, DG, Mitchell, SC, Nash, T and Rhind, S (2000). Gamma interferon influences intestinal epithelial hyperplasia caused by Lawsonia intracellularis infection in mice. Infection and Immunity 68: 6737–6743.Google Scholar
Smith, DGE (2001). Characteristics of Lawsonia intracellularis pathogenesis: recent research and potential benefits. The Pig Journal 47: 98–104.Google Scholar
Smith, DGE and Lawson, GHK (2001). Lawsonia intracellularis: getting inside the pathogenesis of proliferative enteropathy. Veterinary Microbiology 82: 331–345.Google Scholar
Stege, H, Jensen, T, Moller, K, Boekbo, P and Jorsal, S (2000). Prevalence of intestinal pathogens in Danish finishing pig herds. Preventative Veterinary Medicine 46: 279–292.Google Scholar
Stege, H, Jensen, TK, Moller, K, Vestegaard, K, Baekbo, P and Jorsal, SE (2004). Infection dynamics of Lawsonia intracellularis in pig herds. Veterinary Microbiology 104: 197–206.Google Scholar
Stills, HF (1991). Isolation of an intracellular bacterium from hamsters (Mesocricetus auratus) with proliferative ileitis and reproduction of the disease with a pure culture. Infection and Immunity 59: 3227–3236.Google Scholar
Su, H, Messer, R, Whitmire, W, Hughes, S and Caldwell, HD (2000). Subclinical chlamydial infection of the female mouse genital tract generates a potent protective immune response: implications for development of a live attenuated chlamydial vaccine strains. Infection and Immunity 68: 192–196.CrossRefGoogle ScholarPubMed
Suh, D-K, Lym, S-K, Bae, Y-C, Lee, K-W, Choi, W-P and Song, J-C (2000). Detection of Lawsonia intracellularis in diagnostic specimens by one-step PCR. Journal of Veterinary Science 1: 33–37.Google Scholar
Suto, A, Asano, S, Goto, Y, Murata, J, Mori, T and Adachi, M (2004). Survey of porcine proliferative enteritis in the Tohoku district of Japan. Journal of Veterinary Medical Science 66: 547–549.Google Scholar
Todd, WJ, Burgdorfer, W, Marvos, AJ and Wray, GP (1981). Ultrastructural analysis of Rickettsia ricketsii in cultures of persistently infected Vole cells. In: Anacker, WBATL (ed.) Rickettsia and Rickettsial Diseases. London: Academic Press, pp. 255–280.Google Scholar
Tomanova, K and Smola, J (2004). Use of a nested PCR for detection of Lawsonia intracellularis in swine and the number of infected farms in the Czech Republic. In: Proceedings of the 18th International Pig Veterinary Society Congress, Hamburg, Germany, pp. 319.Google Scholar
Vandenburghe, J, Verheyen, A, Lauwers, S and Geboes, K (1985). Spontaneous adenocarcinoma of the ascending colon in Wistar rats: the intracytoplastic presence of a Campylobacter-like bacterium. Journal of Comparative Pathology 95: 45–55.Google Scholar
Vestergaard, K, Stege, H, Baekbo, P, Jensen, TK, Jorsal, SE and Moller, K (2004). Infection dynamics of Lawsonia intra-cellularis in Danish pig herds. In: Proceedings of the 18th IPVS Congress, Hamburg, Germany, pp. 292.Google Scholar
Walter, D, Knittel, J, Schwartz, K, Kroll, J and Roof, M (2000a). Effectiveness of tiamulin in feed for the control and treatment of porcine proliferative enteropathy (ileitis) due to Lawsonia intracellularis infection. In: The 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 75.Google Scholar
Walter, D, Knittel, J, Schwartz, K, Kroll, J and Roof, M (2000b). Effectiveness of tiamulin in drinking water for treatment and control of porcine proliferative enteropathy (ileitis) due to Lawsonia intracellularis infection. In: The 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 31.Google Scholar
Ward, GE and Winkelman, NL (1990). Recognizing the three forms of PE in swine. Veterinary Medicine 85: 197–203.Google Scholar
Watarai, M, Yamato, Y, Horiuchi, N, Kim, S, Omata, Y, Shirahata, T and Furuoka, H (2004). Enzyme-linked immunosorbent assay to detect Lawsonia intracellularis in rabbits with proliferative enteropathy. Veterinary Medicine and Science 66: 735–737.CrossRefGoogle ScholarPubMed
Watarai, M, Yamato, Y, Murakata, K, Kim, S, Omata, Y and Furuoka, H (2005). Detection of Lawsonia intracellularis using immunomagnetic beads and ATP bioluminescence. Journal of Veterinary Medical Science 67: 449–451.Google Scholar
Weber, NL, Beckler, DC, Kapur, V and Gebhart, CJ (2004). Variable number tandem repeat analysis for the differentiation of Lawsonia intracellularis from various animal species. A poster presented internally to the faculty and staff at the University of Minnesota, Minneapolis-St. Paul, MN, USA.Google Scholar
Wendt, M, Bonitz, A and McOrist, S (2004). Prevalence of Lawsonia intracellularis in diagnostic samples from Germany, the Netherlands and Belgium. In: Proceedings of the 17th International Pig Veterinary Society Congress, Ames, IA, USA, pp. 27.Google Scholar
Williams, N, Harrison, L and Gebhart, CJ (1996). Proliferative enteropathy in a foal caused by Lawsonia intracellularis-like bacterium. Journal of Veterinary Diagnostic Investigation 8: 254–256.CrossRefGoogle Scholar
Winkelman, NL (1996). Use of a challenge model to measure the impact of subclinical porcine proliferative enteritis on growth performance in pigs. In: Proceedings of the American Association of Swine Practitioners, pp. 209–211.Google Scholar
Winkelman, NL, Gebhart, C, Collins, J, King, V, Hannon, M and Wolff, T (1997). An evaluation of AUREOMYCIN chlortetracycline (CTC) granular feed additive for prevention of treatment of swine ileitis. In: Proceedings of the American Association of Swine Practitioners, Quebec, Canada, pp. 79–83.Google Scholar
Winkelman, NL, Pauling, GE, Dick, CP, Brennan, J and Wilson, J (1998). Use of a challenge model to measure the impact of subclinical porcine proliferative enteritis on growth performance in pigs. In: Proceedings of the American Association of Swine Practitioners, pp. 209–211.Google Scholar
Winkelman, NL, Holck, JT, Kesl, L, Turner, V and Luempert, III L (2000a). Dose evaluation of ECONOR (valnemulin hydrochloride) for the control of porcine proliferative enteritis using a Lawsonia intracellularis mucosal homogenate challenge. In: Proceedings of the 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 33.Google Scholar
Winkelman, NL, Holck, JT, Turner, V and Luempert, III L (2000b). Therapeutic impact of ECONOR (valnemulin hydrochloride) on the development of porcine proliferative enteritis when supplied simultaneous to Lawsonia intra-cellularis challenge. In: Proceedings of the 16th International Pig Veterinary Society Congress, Melbourne, Australia, pp. 70.Google Scholar
Winkelman, NL, Crane, JP, Elfring, GD, Kratzer, DD, Meeuwse, DM, Dame, KJ, Buckham, SL and Gebhart, CJ (2002). Lincomycin-medicated feed for the control of porcine proliferative enteropathy (ileitis) in swine. Journal of Swine Health and Production 10: 107–111.Google Scholar
Winkelman, NL, Kinsley, K, Gebhart, C and Scherbring, E (2004). Effectiveness of Lawsonia intracellularis specific chicken egg antibody to control ileitis in a swine disease challenge model. In: Proceedings of the 18th International Pig Veterinary Society Congress, Hamburg, Germany, pp. 257.Google Scholar
Zhang, P, Gebhart, CJ, Burden, D and Duhamel, GE (2000). Improved diagnosis of porcine proliferative enteropathy caused by Lawsonia intracellularis using polymerase chain reaction-enzyme-linked oligosorbent assay (PCR-ELOSA). Molecular and Cellular Probes 14: 101–108.CrossRefGoogle ScholarPubMed
Zmudzki, J, Stankevicus, A and Zygmunt, P (2004). Detection of Brachyspira hyodysenteriae and Lawsonia intracellularis in faeces and mucosal specimens by multiplex polymerase chain reaction. In: Proceedings of the 18th International Pig Veterinary Society Congress, Hamburg, Germany, pp. 299.Google Scholar