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Comparative pathology and pathogenesis of naturally acquired and experimentally induced colonic spirochetosis

Published online by Cambridge University Press:  28 February 2007

Gerald E. Duhamel
Gerald E. Duhamel*
Affiliation:
Department of Veterinary and Biomedical Sciences, University of Nebraska-Lincoln Lincoln, Nebraska, USA
*
Room 147, Veterinary Basic Science Building, Department of Veterinary and Biomedical Sciences, University of Nebraska-Lincoln, Lincoln, NE 68583–0905, USA. E-mail: GDUHAMEL1@unl.edu
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Abstract

Research in the past decade has led to the recognition of Brachyspira (formerly Serpulina) pilosicoli as the primary etiologic agent of colonic spirochetosis (CS), an emerging cause of colitis in humans and animals. Attachment of spirochetes to the epithelial surface of the lower intestine is considered to be the hallmark of CS. However, because B. pilosicoli, B. aalborgi and unclassified flagellated bacteria are found singly or together in humans and non-human primates with CS lesions, attachment of spiral-shaped bacteria may not represent the same etiopathogenetic entity in all hosts. Moreover, North American opossums with CS are infected with B. aalborgi-like spirochetes together with flagellated bacteria, whereas B. pilosicoli is found alone in dogs, pigs, chickens and other species of birds with CS. Conversely, guinea-pigs with CS have unidentified spirochetes that may be B. pilosicoli or B. aalborgi. The pig model of CS suggests that attachment of B. pilosicoli to epithelial cells may be transient. By contrast, persistence of B. pilosicoli in the cecal and colonic crypt lumina, chronic inflammation caused by spirochetal invasion into the subepithelial lamina propria and translocation to extraintestinal sites may be more important than previously thought. This review describes the lesions seen in naturally occurring and experimentally induced CS of animals, and it sets the stage for future research into the pathogenic mechanisms of infection and colitis caused by B. pilosicoli.

Type
Research Article
Information
Animal Health Research Reviews , Volume 2 , Issue 1 , June 2001 , pp. 3 - 18
Copyright
Copyright © CAB International 2001

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References

Andrews, JJ and Hoffman, LJ (1982). A porcine colitis caused by a weakly beta hemolytic treponeme (Treponema innocens?). In: Proceedings of the American Association of Veterinary Laboratory Diagnosticians Nashville, Tennessee pp. 395–402.Google Scholar
Antonakopoulos, G, Newman, J and Wilkinson, M (1982). Intestinal spirochetosis: an electron microscopic study of an unusual case. Histopathology 6: 477–488.CrossRefGoogle ScholarPubMed
Barcellos, DESN, Mathiesen, MR, de Uzeda, M, Kader, IITA and Duhamel, GE (2000). Prevalence of Brachyspira (formerly Serpulina) species isolated from diarrhoeic pigs in Brazil. Veterinary Record 146: 398–403.CrossRefGoogle ScholarPubMed
Beer, RJ and Rutter, JM (1972). Spirochaetal invasion of the colonic mucosa in a syndrome resembling swine dysentery following experimental Trichuris suis infection in weaned pigs. Research in Veterinary Science 13: 593–595.CrossRefGoogle Scholar
Blaha, T (1983). Beitrag zur Epizootiologie der Schweinedysenterie – die Ratte als das mögliche Erregerreservoir. Zentralblatt für Veterinärmedizin Reihe B 30: 141–144.CrossRefGoogle Scholar
Burns, DG and Hayes, MM (1985). Rectal spirochaetosis – symptomatic response to metronidazole and mebendazole. South African Medical Journal 68: 335–336.Google ScholarPubMed
Canale-Parola, E (1978). Motility and chemotaxis of spirochetes. Annual Review of Microbiology 32: 69–99.CrossRefGoogle ScholarPubMed
Chen, XG, Correa, P, Offerhaus, J, Rodriguez, E, Janney, F, Hoffmann, E, Fox, J, Hunter, F and Diavolitsis, S (1986). Ultrastructure of the gastric mucosa harboring Campylobacter-like organisms. American Journal of Clinical Pathology 86: 575–582.CrossRefGoogle ScholarPubMed
Christensen, NH (1998). Isolation of Serpulina pilosicoli from scouring finisher pigs, and control of the scouring with zinc bacitracin. In: Proceedings International Pig Veterinary Society Congress Birmingham, England Vol. 3, p. 418.Google Scholar
Cooper, C, Cotton, DWK, Hudson, MJ, Kirkham, N and Wilmott, FEW (1986). Rectal spirochaetosis in homosexual men: characterization of the organism and pathophysiology. Genitourinary Medicine 62:47–52.Google ScholarPubMed
Cotton, DWK, Kirkham, N and Hicks, DA (1984). Rectal spirochaetosis. British Journal of Venereal Diseases 60: 106–109.Google ScholarPubMed
Cowley, HM and Hill, RR (1985). ‘Intestinal spirochaetosis’ of the vervet monkey. Onderstepoort Journal of Veterinary Research 52: 47–50.Google ScholarPubMed
Craige, JE (1948). Spirochetes associated with dysentery in dogs. Journal of the American Veterinary Medical Association 113: 247–249.Google ScholarPubMed
Dauzan, YR, Merlio, JP, Grelier, P, Fong, HIK, Dachary, D, Goussot, JF and de Mascarel, A (1990). La spirochétose colo-rectale: une entité anatomo-pathologique? Annales de Pathologie 10: 258–261.Google Scholar
Davelaar, FG, Smit, HF, Hovind-Hougen, K, Dwars, RM and Van der Valk, PC (1986). Infectious typhlitis in chickens caused by spirochetes. Avian Pathology 15: 247–258.CrossRefGoogle ScholarPubMed
Davis, CP, Mulcahy, D, Takeuchi, A and Savage, DC (1972). Location and description of spiral-shaped microorganisms in the normal rat cecum. Infection and Immunity 6: 184–192.CrossRefGoogle ScholarPubMed
Duhamel, GE (1997). Intestinal spirochaetes in non-production animals. In: Hampson, DJ and Stanton, TB (eds), Intestinal Spirochaetosis in Domestic Animals and Humans. Wallingford, UK: CAB International, pp. 301–320.Google Scholar
Duhamel, GE (1998). Colonic spirochetosis caused by Serpulina pilosicoli . Large Animal Practice 19: 14–22.Google Scholar
Duhamel, GE (2000). Brachyspira pilosicoli colitis of growing swine. In: Proceeding of the Allen D. Leman Swine Conference Minneapolis, Minnesota, Vol. 27, pp. 77–80.Google Scholar
Duhamel, GE, Muniappa, N, Gardner, I, Anderson, MA, Blanchard, PC, DeBey, BM, Mathiesen, MR and Walker, RL (1995 a). Porcine colonic spirochaetosis: A diarrhoeal disease associated with a newly recognized species of intestinal spirochaetes. Pig Journal 35: 101–110.Google Scholar
Duhamel, GE, Muniappa, N, Mathiesen, MR, Johnson, JL, Toth, J, Elder, RO and Doster, AR (1995 b). Certain canine weakly beta-hemolytic intestinal spirochetes are phenotypically and genotypically related to spirochetes associated with human and porcine intestinal spirochetosis. Journal of Clinical Microbiology 33: 2211–2215.CrossRefGoogle ScholarPubMed
Duhamel, GE, Hunsaker, BD, Mathiesen, MR and Moxley, RA (1996). Intestinal spirochetosis and giardiasis in a Beagle pup with diarrhea. Veterinary Pathology 33: 360–362.CrossRefGoogle Scholar
Duhamel, GE, Elder, RO, Muniappa, N, Mathiesen, MR, Wong, VJ and Tarara, RP (1997). Colonic spirochetal infections in nonhuman primates that were associated with Brachyspira aalborgi, Serpulina pilosicoli, and unclassified flagellated bacteria. Clinical Infectious Disease 25 (Suppl. 2): S186–S188.CrossRefGoogle ScholarPubMed
Duhamel, GE, Ganley, L, Barr, BC, Whipple, JP, Mathiesen, MR, Nordhausen, RW, Walker, RL, Bargar, TW and Van Kruiningen, HJ (1998 a). Intestinal spirochetosis of North American opossums (Didelphis virginiana); a potential biological vector for pathogenic spirochetes. In: Proceedings of the American Association of Zoo Veterinarians and American Association of Wildlife Veterinarians Joint Conference Omaha, Nebraska, pp. 83–88.Google Scholar
Duhamel, GE, Trott, DJ, Muniappa, N, Mathiesen, MR, Tarasiuk, K, Lee, JI and Hampson, DJ (1998 b). Canine intestinal spirochetes consist of Serpulina pilosicoli and a newly identified group provisionally designated ‘Serpulina canis’ sp. nov. Journal of Clinical Microbiology 36: 2264–2270.CrossRefGoogle Scholar
Duhamel, GE, Jensen, TK, Boye, M and Møller, K (2000 a). Pattern of mucosal colonization in naturally-occurring porcine spirochetal colitis as determined by immunohistochemical staining with a Brachyspira FlaB-specific monoclonal antibody. In: Proceedings of the Annual Meeting Conference of Research Workers in Animal Diseases Chicago, Illinois, p. 51P.Google Scholar
Duhamel, GE, Dritz, SS and Hock, JT (2000 b). Dietary modulation of Brachyspira (formerly Serpulina) pilosicoli infection and colitis in a challenge model of porcine colonic spirochetosis. In: Proceedings of the International Pig Veterinary Society Congress Melbourne, Australia, Vol. 1, p. 45.Google Scholar
Dwars, RM, Smit, HF, Davelaar, FG and Van't Veer, W (1989). Incidence of spirochetal infections in cases of intestinal disorders in chickens. Avian Pathology 18: 591–595.CrossRefGoogle ScholarPubMed
Dwars, RM, Davelaar, FG and Smit, HF (1992). Infection of broiler chicks (Gallus domesticus) with human intestinal spirochetes. Avian Pathology 21: 559–568.CrossRefGoogle Scholar
Dytoc, M, Gold, B, Louie, M, Huesca, M, Fedorko, L, Crowe, S, Lingwood, C, Brunton, J and Sherman, P (1993). Comparison of Helicobacter pylori and attaching-effacing Escherichia coli adhesion to eukaryotic cells. Infection and Immunity 61: 448–456.CrossRefGoogle ScholarPubMed
Fellström, C, Pettersson, B, Johansson, KE, Lundeheim, N and Gunnarsson, A (1996). Prevalence of Serpulina species in relation to diarrhea and feed medication in pig rearing herds in Sweden. American Journal of Veterinary Research 57: 807–811.CrossRefGoogle ScholarPubMed
Fellström, C, Pettersson, B, Thomson, J, Gunnarsson, A, Persson, M and Johansson, KE (1997). Identification of Serpulina species associated with porcine colitis by biochemical analysis and PCR. Journal of Clinical Microbiology 35: 462–467.CrossRefGoogle ScholarPubMed
Fellström, C, Karlsson, M, Pettersson, B, Zimmerman, U, Gunnarsson, A and Aspan, A (1999). Emended descriptions of indole negative and indole positive isolates of Brachyspira (Serpulina) hyodysenteriae . Veterinary Microbiology 70: 225–238.CrossRefGoogle ScholarPubMed
Fisher, LN, Mathiesen, MR and Duhamel, GE (1997). Restriction fragment length polymorphism of the periplasmic flagellar flaA1 gene of Serpulina species. Clinical and Diagnostic Laboratory Immunology 4: 681–686.CrossRefGoogle ScholarPubMed
Gebbers, JO, Ferguson, DJ, Mason, C, Kelley, P and Jewell, DP (1987). Spirochaetosis of the human rectum associated with an intraepithelial mast cell and IgE plasma cell response. Gut 28: 588–593.CrossRefGoogle ScholarPubMed
Girard, C, Lemarchand, T and Higgins, R (1995). Porcine colonic spirochetosis: a retrospective study of eleven cases. Canadian Veterinary Journal 36: 291–294.Google ScholarPubMed
Gold, BD, Dytoc, M, Huesca, M, Philpott, D, Kuksis, A, Czinn, S, Lingwood, CA and Sherman, PM (1995). Comparison of Helicobacter mustelae and Helicobacter pylori adhesion to eukaryotic cells in vitro. Gastroenterology 109: 692–700.CrossRefGoogle ScholarPubMed
Gordon, JH and Dubos, R (1970). The anaerobic bacterial flora of the mouse cecum. Journal of Experimental Medicine 132: 251–260.CrossRefGoogle ScholarPubMed
Goudswaard, J and Cornelisse, JL (1973). The agent possibly associated with swine dysentery and the antigenic relationship with Borrelia canis . Veterinary Record 92: 562–563.CrossRefGoogle ScholarPubMed
Griffiths, IB, Hunt, BW, Lister, SA and Lamont, MH (1987). Retarded growth rate and delayed onset of egg production associated with spirochaete infection in pullets. Veterinary Record 121: 35–37.CrossRefGoogle ScholarPubMed
Guccion, JG, Benator, DA, Zeller, J, Termanini, B and Saini, N (1995). Intestinal spirochetosis and acquired immunodeficiency syndrome: ultrastructural studies of two cases. Ultrastructural Pathology 19: 15–22.CrossRefGoogle ScholarPubMed
Hampson, DJ and Trott, DJ (1999). Spirochetal diarrhea/porcine intestinal spirochetosis. In: Straw, BE, D'Allaire, S, Mengeling, WL and Taylor, DJ (eds), Diseases of Swine. Ames: Iowa State University Press, pp. 553–562.Google Scholar
Hampson, DJ, Combs, BG, Harders, SJ, Connaughton, ID and Fahy, VA (1991). Isolation of Treponema hyodysenteriae from a wild rat living on a piggery. Australian Veterinary Journal 68: 308.CrossRefGoogle ScholarPubMed
Hampson, DJ, Robertson, ID and Oxberry, SL (1998 a). Extraintestinal colonisation by Serpulina pilosicoli in an experimentally inoculated pig. In: Proceedings of the International Pig Veterinary Society Congress Birmingham, England, Vol. 2, p. 54.Google Scholar
Hampson, DJ, Robertson, ID, Oxberry, SL and Pethick, DW (1998 b). Evaluation of vaccination and diet for the control of Serpulina pilosicoli infection (porcine intestinal spirochaetosis). In: Proceedings of the International Pig Veterinary Society Congress Birmingham, England, Vol. 2, p. 56.Google Scholar
Harland, WA and Lee, FD (1967). Intestinal spirochaetosis. British Medical Journal 3: 718–719.CrossRefGoogle ScholarPubMed
Hartland, EL, Mikosza, ASJ, Robins-Browne, RM and Hampson, DJ (1998). Examination of Serpulina pilosicoli for attachment and invasion determinants of enterobacteria. FEMS Microbiology Letters 165: 59–63.CrossRefGoogle ScholarPubMed
Heinonen, M, Fossi, M, Jalli, JP, Saloniemi, H and Tuovinen, V (2000). Detectability and prevalence of Brachyspira species in herds rearing health class feeder pigs in Finland. Veterinary Record 146: 343–347.CrossRefGoogle ScholarPubMed
Hommez, J, Castryck, F, Haesebrouck, F and Vevriese, LA (1998). Identification of porcine Serpulina strains in routine diagnostic bacteriology. Veterinary Microbiology 62: 163–169.CrossRefGoogle ScholarPubMed
Hovind-Hougen, K, Birch-Andersen, A, Henrik-Nielsen, R, Orholm, M, Pederse, JO, Teglbjærg, PS and Thaysen, EH (1982). Intestinal spirochetosis: morphological characterization and cultivation of the spirochete Brachyspira aalborgi gen. nov., sp. nov. Journal of Clinical Microbiology 16: 1127–1136.CrossRefGoogle ScholarPubMed
Hughes, R, Olander, HJ and Williams, CB (1975). Swine dysentery: Pathogenicity of Treponema hyodysenteriae . American Journal of Veterinary Research 36: 971–977.Google ScholarPubMed
Jacques, M, Girard, C, Higgins, R and Goyette, G (1989). Extensive colonization of the porcine colonic epithelium by a spirochete similar to Treponema innocens . Journal of Clinical Microbiology 27: 1139–1141.CrossRefGoogle ScholarPubMed
Jensen, TK, Møller, K, Boye, M, Leser, TD and Jorsal, SE (2000). Scanning electron microscopy and fluorescent in situ hybridization of experimental Brachyspira (Serpulina) pilosicoli infection in growing pigs. Veterinary Pathology 37: 22–32.CrossRefGoogle ScholarPubMed
Joens, LA (1980). Experimental transmission of Treponema hyo-dysenteriae from mice to pigs. American Journal of Veterinary Research 41: 1225–1226.Google ScholarPubMed
Joens, LA and Kinyon, JM (1982). Isolation of Treponema hyo-dysenteriae from wild rodents. Journal of Clinical Microbiology 15: 994–997.CrossRefGoogle ScholarPubMed
Joens, LA, Songer, JG, Harris, DL and Glock, RD (1978). Experimental infection with Treponema hyodysenteriae in guinea pigs. Infection and Immunity 22: 132–135.CrossRefGoogle ScholarPubMed
Johnston, T, Duhamel, GE, Mathiesen, MR, Walter, D, Smart, N and Dewey, C (1999). Recent advances in diagnosing and controlling porcine colonic spirochetosis. Compendium on Food Animal Health Management 21: S198–S207.Google Scholar
Jones, MJ, Miller, JM and George, WL (1986). Microbiological and biochemical characterization of spirochetes isolated from the feces of homosexual males. Journal of Clinical Microbiology 24: 1071–1074.CrossRefGoogle ScholarPubMed
Kinyon, JM and Harris, DL (1979). Treponema innocens, a new species of intestinal bacteria, and emended description of the type strain of Treponema hyodysenteriae Harris et al . International Journal of Systematic Bacteriology 29: 102–109.CrossRefGoogle Scholar
Kinyon, JM, Harris, DL and Glock, RD (1977). Enteropathogenicity of various isolates of Treponema hyo-dysenteriae . Infection and Immunity 15: 638–646.CrossRefGoogle Scholar
Koopman, MBH, Käsbohrer, A, Beckmann, G, van der Zeijst, BAM and Kusters, JG (1993). Genetic similarity of intestinal spirochetes from humans and various animal species. Journal of Clinical Microbiology 31: 711–716.CrossRefGoogle ScholarPubMed
Kraaz, W, Pettersson, B, Thunberg, U, Engstrand, L and Fellström, C (2000). Brachyspira aalborgi infection diagnosed by culture and 16S ribosomal DNA sequencing using human colonic biopsy specimens. Journal of Clinical Microbiology 38: 3555–3560.CrossRefGoogle ScholarPubMed
Law, CLH, Grierson, JM and Stevens, SMB (1994). Rectal spirochaetosis in homosexual men: the association with sexual practices, HIV infection and enteric flora. Genitourinary Medicine 70: 26–29.Google ScholarPubMed
Leach, WD, Lee, A and Stubbs, RP (1973). Localization of bacteria in the gastrointestinal tract: A possible explanation of intestinal spirochaetosis. Infection and Immunity 7: 961–972.CrossRefGoogle ScholarPubMed
Lee, A, Gordon, J and Dubos, R (1968). Enumeration of the oxygen sensitive bacteria usually present in the intestine of healthy mice. Nature 220: 1137–1139.CrossRefGoogle ScholarPubMed
Lee, A, Gordon, J, Lee, CJ and Dubos, R (1971). The mouse intestinal microflora with emphasis on the strict anaerobes. Journal of Experimental Medicine 133: 339–352.CrossRefGoogle ScholarPubMed
Lee, JI and Hampson, DJ (1994). Genetic characterisation of intestinal spirochaetes and their association with disease. Journal of Medical Microbiology 40: 365–371.CrossRefGoogle ScholarPubMed
Lee, JI and Hampson, DJ (1996). The prevalence of intestinal spirochaetes in dogs. Australian Veterinary Journal 74: 25–26.CrossRefGoogle ScholarPubMed
Lee, JI, Hampson, DJ, Lymbery, AJ and Harders, SJ (1993). The porcine intestinal spirochaetes: identification of new genetic groups. Veterinary Microbiology 34: 273–285.CrossRefGoogle ScholarPubMed
Lindboe, CF, Tostrup, NE, Nersund, R and Rekkavik, G (1993). Human intestinal spirochaetosis in Mid-Norway. Acta Pathologia Microbiologia Immunologia Scandinavia 101: 858–864.CrossRefGoogle ScholarPubMed
Macfie, JWS (1916). The morphology of certain spirochaetes of man and other animals. Annals of Tropical Medicine and Parasitology 10: 305–343.CrossRefGoogle Scholar
Marshall, T and Allen, A (1978). The isolation and characterization of the high-molecular-weight glycoprotein from pig colonic mucus. Biochemistry Journal 173: 569–578.CrossRefGoogle ScholarPubMed
McLaren, AJ, Trott, DJ, Swayne, DE, Oxberry, SL and Hampson, DJ (1997). Genetic and phenotypic characterization of intestinal spirochetes colonizing chickens and allocation of known pathogenic isolates to three distinct genetic groups. Journal of Clinical Microbiology 35: 412–417.CrossRefGoogle ScholarPubMed
McLeod, CG, Stookey, JL, Harrington, DG and White, JD (1977). Intestinal Tyzzer's disease and spirochetosis in a guinea pig. Veterinary Pathology 14: 229–235.CrossRefGoogle Scholar
Mikosza, ASJ, La, T, Brooke, CJ, Lindboe, CF, Ward, PB, Heine, RG, Guccion, JG, de Boer, WB and Hampson, DJ (1999). PCR amplification from fixed tissue indicates frequent involvement of Brachyspira aalborgi in human intestinal spirochetosis. Journal of Clinical Microbiology 37: 2093–2098.CrossRefGoogle ScholarPubMed
Mikosza, ASJ, La, T, de Boer, WB and Hampson, DJ (2001). Comparative prevalences of Brachyspira aalborgi and Brachyspira (Serpulina) pilosicoli as etiologic agents of histologically identified intestinal spirochetosis in Australia. Journal of Clinical Microbiology 39: 347–350.CrossRefGoogle ScholarPubMed
Moon, HW, Whipp, SC, Argenzio, RA, Levine, MM and Gianella, RA (1983). Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infection and Immunity 41: 1340–1351.CrossRefGoogle ScholarPubMed
Moxley, RA and Duhamel, GE (1999). Comparative pathology of enteric bacterial diseases of swine. Advances in Experimental Medicine and Biology 473: 83–101.CrossRefGoogle ScholarPubMed
Muniappa, N and Duhamel, GE (1997). Outer membrane-associated serine protease of intestinal spirochetes. FEMS Microbiology Letters 154: 159–164.CrossRefGoogle ScholarPubMed
Muniappa, N, Duhamel, GE, Mathiesen, MR and Bargar, TW (1996). Light microscopic and ultrastructural changes in the ceca of chicks inoculated with human and canine Serpulina pilosicoli . Veterinary Pathology 33: 542–550.CrossRefGoogle ScholarPubMed
Muniappa, N, Mathiesen, MR and Duhamel, GE (1997). Laboratory identification and enteropathogenicity testing of Serpulina pilosicoli associated with porcine colonic spirochetosis. Journal of Veterinary Diagnostic Investigation 9: 165–171.CrossRefGoogle ScholarPubMed
Muniappa, N, Ramanathan, MR, Tarara, RP, Westerman, RB, Mathiesen, MR and Duhamel, GE (1998). Attachment of human and rhesus Serpulina pilosicoli to cultured cells and comparison with a chick infection model. Journal of Spirochetal and Tick-borne Diseases 5: 44–53.Google Scholar
Neef, NA, Lysons, RJ, Trott, DJ, Hampson, DJ, Jones, PW and Morgan, JH (1994). Pathogenicity of porcine intestinal spirochetes in gnotobiotic pigs. Infection and Immunity 62: 2395–2403.CrossRefGoogle ScholarPubMed
Neutra, MR (1980). Prokaryotic – eukaryotic cell junctions: Attachment of spirochetes and flagellated bacteria to primate large intestinal cells. Journal of Ultrastructural Research 70: 186–203.CrossRefGoogle ScholarPubMed
Nielsen, RH, Orholm, M, Pedersen, JO, Hovind-Hougen, K, Teglbjærg, PS and Thaysen, EH (1983). Colorectal spiro-chetosis: Clinical significance of the infestation. Gastroenterology 85: 62–67.CrossRefGoogle ScholarPubMed
Noach, LA, Rolf, TM and Tytgat, GNJ (1994). Electron microscopic study of association between Helicobacter pylori and gastric and duodenal mucosa. Journal of Clinical Pathology 47: 699–704.CrossRefGoogle ScholarPubMed
Ochiai, S, Adachi, Y and Mori, K (1997). Unification of the genera Serpulina and Brachyspira, and proposals of Brachyspira hyodysenteriae comb. nov., Brachyspira innocens comb. nov. and Brachyspira pilosicoli comb. nov. Microbiology and Immunology 41: 445–452.CrossRefGoogle ScholarPubMed
Oxberry, SL, Trott, DJ and Hampson, DJ (1998). Serpulina pilosi-coli, waterbirds and water: potential sources of infection for humans and other animals. Epidemiology and Infection 121: 219–225.CrossRefGoogle ScholarPubMed
Padmanabhan, V, Dahlstrom, J, Maxwell, L, Kaye, G, Clarke, A and Barratt, PJ (1996). Invasive intestinal spirochetosis: A report of three cases. Pathology 28: 283–286.CrossRefGoogle ScholarPubMed
Park, NY, Chung, CY, McLaren, AJ, Atyeo, RF and Hampson, DJ (1995). Polymerase chain reaction for identification of human and porcine spirochaetes recovered from cases of intestinal spirochaetosis. FEMS Microbiology Letters 125: 225–230.CrossRefGoogle ScholarPubMed
Pearson, GR, Skelton-Stroud, PN and Orford, CR (1985). Observations by light microscopy and transmission electron microscopy on intestinal spirochetosis in baboons (Papio spp.). Journal of Medical Microbiology 19: 359–366.CrossRefGoogle ScholarPubMed
Pindak, FF, Clapper, WE and Sherrod, JH (1965). Incidence and distribution of spirochetes in the digestive tract of dogs. American Journal of Veterinary Research 26: 1391–1402.Google ScholarPubMed
Pluske, JR, Durmic, Z, Pethick, DW, Mullan, BP and Hampson, DJ (1998). Confirmation of the role of rapidly fermentable carbohydrates in the expression of swine dysentery in pigs after experimental infection. Journal of Nutrition 128: 1737–1744.CrossRefGoogle ScholarPubMed
Ramanathan, M, Duhamel, GE, Mathiesen, MR and Messier, S (1993). Identification and partial characterization of a group of weakly β-hemolytic intestinal spirochetes of swine distinct from Serpulina innocens, isolate B256. Veterinary Microbiology 37: 53–64.CrossRefGoogle ScholarPubMed
Rodgers, FG, Rodgers, C, Shelton, AP and Hawkey, CJ (1986). Proposed pathogenic mechanism for the diarrhea associated with human intestinal spirochetes. American Journal of Clinical Pathology 86: 679–682.CrossRefGoogle ScholarPubMed
Ruane, PJ, Nakata, MM, Reinhardt, JF and George, WL (1989). Spirochete-like organisms in the human gastrointestinal tract. Reviews of Infectious Diseases 11: 184–196.CrossRefGoogle ScholarPubMed
Sacco, RE, Trampel, DW and Wannemuehler, MJ (1997). Experimental infection of C3H mice with avian, porcine, or human isolates of Serpulina pilosicoli . Infection and Immunity 65: 5349–5353.CrossRefGoogle ScholarPubMed
Savage, DC (1972). Associations and physiological interactions of indigenous microorganisms and gastrointestinal epithe-lia. American Journal of Clinical Nutrition 25: 1372–1379.CrossRefGoogle Scholar
Savage, DC, McAllister, JS and Davis, CP (1971). Anaerobic bacteria on the mucosal epithelium of the murine large bowel. Infection and Immunity 4: 492–502.CrossRefGoogle ScholarPubMed
Shera, AG (1962). Specific granular lesions associated with intestinal spirochaetosis. British Journal of Surgery 50: 68–77.CrossRefGoogle ScholarPubMed
Siba, PM, Pethick, DW and Hampson, DJ (1996). Pigs experimentally infected with Serpulina hyodysenteriae can be protected from developing swine dysentary by feeding them a highly digestible diet. Epidemiology and Infection 116: 207–216.CrossRefGoogle Scholar
Spearman, JG, Nayar, G and Sheridan, M (1988). Colitis associated with Treponema innocens in pigs. Canadian Veterinary Journal 29: 747.Google ScholarPubMed
Stanton, TB, Fournié-Amazouz, E, Postic, D, Trott, DJ, Grimont, PAD, Baranton, G, Hampson, DJ and Saint Girons, I (1997). Recognition of two new species of intestinal spirochetes: Serpulina intermedia sp. nov. and Serpulina murdochii sp. nov. International Journal of Systematic Bacteriology 47: 1007–1012.CrossRefGoogle ScholarPubMed
Stoutenburg, JE, Swayne, DE, Hoepf, TM, Wack, R and Kramer, L (1995). Frequency of intestinal spirochetes in birds, rats, and pigs from a zoological collection and private rhea farms in Ohio. Journal of Zoo and Wildlife Medicine 26: 272–278.Google Scholar
Surawicz, CM (1995). Colorectal spirochetosis. In: Surawicz, CM and Owen, R (eds), Gastrointestinal and Hepatic Infections. Philadelphia: WB Saunders Co., pp. 287–293.Google Scholar
Swayne, DE and McLaren, AJ (1997). Avian intestinal spirochaetes and avian intestinal spirochaetosis. In: Hampson, DJ and Stanton, TB (eds), Intestinal Spirochaetosis in Domestic Animals and Humans. Wallingford, UK: CAB International, pp. 267–300.Google Scholar
Takeuchi, A and Zeller, JA (1972 a). Scanning electron microscopic observations on the surface of the normal and spirochete-infected colonic mucosa of the rhesus monkey. Journal of Ultrastructural Research 40: 313–324.CrossRefGoogle Scholar
Takeuchi, A and Zeller, JA (1972 b). Ultrastructural identification of spirochetes and flagellated microbes at the brush border of the large intestinal epithelium of the rhesus monkey. Infection and Immunity 6: 1008–1018.CrossRefGoogle ScholarPubMed
Takeuchi, A, Jervis, HR, Nakazawa, H and Robinson, DM (1974). Spiral-shaped organisms on the surface colonic epithelium of the monkey and man. American Journal of Clinical Nutrition 27: 1287–1296.CrossRefGoogle ScholarPubMed
Taylor, DJ (1999). Spirochaetal diarrhoea. In: Taylor, DJ (ed.), Pig Diseases. Bury St Edmunds: St Edmundsbury Press Ltd, pp. 166–169.Google Scholar
Taylor, DJ, Simmons, JR and Laird, HM (1980). Production of diarrhea and dysentery in pigs by feeding pure cultures of a spirochete differing from Treponema hyodysenteriae . Veterinary Record 106: 326–332.CrossRefGoogle ScholarPubMed
Teglbjærg, PS (1990). Intestinal spirochetosis. In: Williams, GT (ed.), Gastrointestinal Pathology. Berlin: Springer-Verlag, pp. 247–256.CrossRefGoogle Scholar
Thomson, JR, Smith, WJ, Murray, BP and McOrist, S (1997). Pathogenicity of three strains of Serpulina pilosicoli in pigs with a naturally acquired intestinal flora. Infection and Immunity 65: 3693–3700.CrossRefGoogle ScholarPubMed
Thomson, JR, Smith, WJ and Murray, BP (1998). Investigations into field cases of porcine colitis with particular reference to infection with Serpulina pilosicoli . Veterinary Record 142: 235–239.CrossRefGoogle ScholarPubMed
Trampel, DW, Jensen, NS and Hoffman, LJ (1994). Cecal spiro-chetosis in commerical laying hens. Avian Diseases 38: 895–898.CrossRefGoogle Scholar
Trivett-Moore, NL, Gilbert, GL, Law, CH, Trott, DJ and Hampson, DJ (1998). Isolation of Serpulina pilosicoli from rectal biopsy specimens showing evidence of intestinal spirochetosis. Journal of Clinical Microbiology 36: 261–265.CrossRefGoogle ScholarPubMed
Trott, DJ and Hampson, DJ (1998). Evaluation of day-old spe-cific pathogen-free chicks as an experimental model for pathogenicity testing of intestinal spirochaete species. Journal of Comparative Pathology 118: 365–381.CrossRefGoogle Scholar
Trott, DJ, McLaren, AJ and Hampson, DJ (1995). Pathogenicity of human and porcine intestinal spirochetes in one-day-old specific-pathogen-free chicks: an animal model of intestinal spirochetosis. Infection and Immunity 63: 3705–3710.CrossRefGoogle ScholarPubMed
Trott, DJ, Stanton, TB, Jensen, NS, Duhamel, GE, Johnson, JL and Hampson, DJ (1996 a). Serpulina pilosicoli sp. nov., the agent of porcine intestinal spirochetosis. International Journal of Systematic Bacteriology 46: 206–215.CrossRefGoogle ScholarPubMed
Trott, DJ, Atyeo, RF, Lee, JI, Swayne, DA, Stoutenburg, JW and Hampson, DJ (1996 b). Genetic relatedness amongst intestinal spirochaetes isolated from rats and birds. Letters in Applied Microbiology 23: 431–436.CrossRefGoogle ScholarPubMed
Trott, DJ, Huxtable, CR and Hampson, DJ (1996 c). Experimental infection of newly weaned pigs with human and porcine strains of Serpulina pilosicoli . Infection and Immunity 64: 4648–4654.CrossRefGoogle ScholarPubMed
Trott, DJ, Stanton, TB, Jensen, NS and Hampson, DJ (1996 d). Phenotypic characteristics of Serpulina pilosicoli the agent of intestinal spirochaetosis. FEMS Microbiology Letters 142: 209–214.CrossRefGoogle ScholarPubMed
Trott, DJ, Jensen, NS, Saint Girons, I, Oxberry, SL, Stanton, TB, Lindquist, D and Hampson, DJ (1997 a). Identification and characterization of Serpulina pilosicoli isolates recovered from the blood of critically ill patients. Journal of Clinical Microbiology 35: 482–485.CrossRefGoogle ScholarPubMed
Trott, DJ, Combs, BG, Mikosza, ASJ, Oxberry, SL, Robertson, ID, Passey, M, Taime, J, Sehuko, R, Alpers, MP and Hampson, DJ (1997 b). The prevalence of Serpulina pilosicoli in humans and domestic animals in the Eastern Highlands of Papua New Guinea. Epidemiology and Infection 119: 369–379.CrossRefGoogle ScholarPubMed
Trott, DJ, Mikosza, ASJ, Combs, BG, Oxberry, SL and Hampson, DJ (1998). Population genetic analysis of Serpulina pilosi-coli and its molecular epidemiology in villages in the Eastern Highlands of Papua New Guinea. International Journal of Systematic Bacteriology 48: 659–668.CrossRefGoogle ScholarPubMed
Turek, JJ and Meyer, RC (1977). Studies on a canine intestinal spirochete I. Its isolation, cultivation, and ultrastructure. Canadian Journal of Comparative Medicine 41: 332–337.Google ScholarPubMed
Turek, JJ and Meyer, RC (1978). Studies on a canine intestinal spirochete: Scanning electron microscopy of canine colonic mucosa. Infection and Immunity 20: 853–855.CrossRefGoogle ScholarPubMed
Turek, JJ and Meyer, RC (1979). An intestinal spirochete infestation in the opossum. Current Microbiology 3: 27–31.CrossRefGoogle Scholar
Vanrobaeys, M, De Herdt, P, Ducatelle, R, Devriese, LA, Charlier, G and Haesebrouck, F (1998). Typhlitis by intestinal Serpulina-like bacteria in domestic guinea pigs (Cavia porcellus). Journal of Clinical Microbiology 36: 690–694.CrossRefGoogle ScholarPubMed
Webb, DM, Duhamel, GE, Mathiesen, MR, Muniappa, N and White, AK (1997). Cecal spirochetosis associated with Serpulina pilosicoli in captive juvenile ring-necked pheasants. Avian Diseases 41: 997–1002.CrossRefGoogle ScholarPubMed
Weber, VA and Schramm, R (1989). Untersuchungen zum vorkommen von Treponemen in Kotproben von Hunden und Katzen mit und ohne Darmerkrankungen. Berliner und Münchener Tierärztliche Wochenschrift 102: 73–77.Google Scholar
White, A, Hansen-Lardy, L, Brodersen, B, Kelling, CL, Hesse, R and Duhamel, GE (1998). Enhanced immunohistochemical detection of infectious agents in formalin-fixed, paraffin-embedded tissues following heat mediated antigen retrieval. Journal of Veterinary Diagnostic Investigation 10: 214–217.CrossRefGoogle ScholarPubMed
White, J, Roche, D, Chan, YF and Mitchell, EA (1994). Intestinal spirochetosis in children: report of two cases. Pediatric Pathology 14: 191–199.CrossRefGoogle ScholarPubMed
Witters, NA and Duhamel, GE (1999). Motility-regulated mucin association of Serpulina pilosicoli, the agent of colonic spirochetosis of humans and animals. Advances in Experimental Medicine and Biology 473: 199–205.CrossRefGoogle ScholarPubMed
Zhang, P, Cheng, X and Duhamel, GE (2000). Cloning and DNA sequence analysis of an immunogenic glucose/galactose MglB lipoprotein homologue from Brachyspira pilosicoli, the agent of colonic spirochetosis. Infection and Immunity 68: 4559–4565.CrossRefGoogle ScholarPubMed
Zwicker, GM, Dagle, GE and Adee, RR (1978). Naturally occurring Tyzzer's disease and intestinal spirochetosis in guinea pigs. Laboratory Animal Science 28: 193–198.Google ScholarPubMed
Zymet, CL (1969). Canine spirochetosis and its association with diarrhea. Veterinary Medicine and Small Animal Clinician 64: 883–887.Google ScholarPubMed