The comparative pathology of Clostridium difficile-associated disease

Veterinary Pathology

Volumn 43, Issue 3, 2006, Pages 225-240

  Keel, M K ^a   Songer, J G ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Antibiotic associated diarrhea; Clostridium difficile; Colitis; Enteritis; Exotoxin; TcdA; TcdB; Typhlocolitis

Indexed keywords

ANIMAL; ANIMAL DISEASE; CLOSTRIDIUM DIFFICILE; DISEASE PREDISPOSITION; INTESTINE; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PSEUDOMEMBRANOUS COLITIS; REVIEW;

ANIMAL DISEASES; ANIMALS; CLOSTRIDIUM DIFFICILE; DISEASE SUSCEPTIBILITY; ENTEROCOLITIS, PSEUDOMEMBRANOUS; INTESTINES;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM DIFFICILE; EQUIDAE; EQUUS CABALLUS; MAMMALIA; MESOCRICETUS AURATUS; ORYCTOLAGUS CUNICULUS; SUS SCROFA;

EID: 33646439545     PISSN: 03009858     EISSN: 03009858     Source Type: Journal    
DOI: 10.1354/vp.43-3-225     Document Type: Review

References (170)

1. Alcantara C, Stenson WF, Steiner TS, Guerrant RL: Role of inducible cyclooxygenase and prostaglandins in Clostridium difficile toxin A-induced secretion and inflammation in an animal model. J Infect Dis 184:648-652, 2001
2. Arnon SS, Mills DC, Day PA, Henrickson RV, Sullivan NM, Wilkins TD: Rapid death of infant rhesus monkeys injected with Clostridium difficile toxins A and B: physiologic and pathologic basis. J Pediatr 104:34-40, 1984
3. Bacon KB, Flores-Romo L, Aubry JP, Wells TN, Power CA: Interleukin-8 and RANTES induce the adhesion of the human basophilic cell line KU-812 to human endothelial cell monolayers. Immunology 82:473-481, 1994
4. Bartlett JG, Chang TW, Moon N, Onderdonk AB: Antibiotic-induced lethal enterocolitis in hamsters: studies with eleven agents and evidence to support the pathogenic role of toxin-producing Clostridia. Am J Vet Res 39:1525-1530, 1978
5. Baverud V, Franklin A, Gunnarsson A, Gustafsson A, Hellander-Edman A: Clostridium difficile associated with acute colitis in mares when their foals are treated with erythromycin and rifampicin for Rhodococcus equi pneumonia. Equine Vet J 30:482-488, 1998
6. Baverud V, Gustafsson A, Franklin A, Aspan A, Gunnarsson A: Clostridium difficile: prevalence in horses and environment, and antimicrobial susceptibility. Equine Vet J 35:465-471, 2003
7. Baverud V, Gustafsson A, Franklin A, Lindholm A, Gunnarsson A: Clostridium difficile associated with acute colitis in mature horses treated with antibiotics. Equine Vet J 29:279-284, 1997
8. Berry AP, Levett PN: Chronic diarrhoea in dogs associated with Clostridium difficile infection. Vet Rec 118:102-103, 1986
9. Bignardi GE: Risk factors for Clostridium difficile infection. J Hosp Infect 40:1-15, 1998
10. Black PH: Stress and the inflammatory response: a review of neurogenic inflammation. Brain Behav Immun 16:622-653, 2002
11. Blake JE, Mitsikosta F, Metcalfe MA: Immunological detection and cytotoxic properties of toxins from toxin A-positive, toxin B-positive Clostridium difficile variants. J Med Microbiol 53:197-205, 2004
12. Blankenship-Paris TL, Walton BJ, Hayes YO, Chang J: Clostridium difficile infection in hamsters fed an atherogenic diet. Vet Pathol 32:269-273, 1995
13. Bolton RP, Tait SK, Dear PR, Losowsky MS: Asymptomatic neonatal colonisation by Clostridium difficile. Arch Dis Child 59:466-472, 1984
14. Borriello SP: Clostridial disease of the gut. Clin Infect Dis 20 (Suppl 2): S242-S250, 1995
15. Borriello SP, Carman RJ: Association of iota-like toxin and Clostridium spiroforme with both spontaneous and antibiotic-associated diarrhea and colitis in rabbits. J Clin Microbiol 17:414-418, 1983
16. Borriello SP, Honour P, Turner T, Barclay F: Household pets as a potential reservoir for Clostridium difficile infection. J Clin Pathol 36:84-87, 1983
17. Borriello SP, Welch AR, Barclay FE, Davies HA: Mucosal association by Clostridium difficile in the hamster gastrointestinal tract. J Med Microbiol 25:191-196, 1988
18. Borriello SP, Wilcox MH: Clostridium difficile infections of the gut: the unanswered questions. J Antimicrob Chemother 41 (Suppl C):67-69, 1998
19. Brooks ME, Sterne M, Warrack GH: A reassessment of the criteria used for type differentiation of Clostridium perfringens. J Pathol Bacteriol 74:185-195, 1957
20. Buck AC, Cooke EM: The fate of ingested Pseudomonas aeruginosa in normal persons. J Med Microbiol 2:521-525, 1969
21. Bueschel D, Walker R, Woods L, Kokai-Kun J, McClane B, Songer JG: Enterotoxigenic Clostridium perfringens type A necrotic enteritis in a foal. J Am Vet Med Assoc 213:1305-1307, 1280, 1998
22. Carman RJ, Borriello SP: Infectious nature of Clostridium spiroforme-mediated rabbit enterotoxaemia. Vet Microbiol 9:497-502, 1984
23. Carman RJ, Borriello SP: Laboratory diagnosis of Clostridium spiroforme-mediated diarrhoea (iota enterotoxaemia) of rabbits. Vet Rec 113:184-185, 1983
24. Carman RJ, Evans RH: Experimental and spontaneous clostridial enteropathies of laboratory and free living lagomorphs. Lab Anim Sci 34:443-452, 1984
25. Castagliuolo I, Keates AC, Wang CC, Pasha A, Valenick L, Kelly CP, Nikulasson ST, LaMont JT, Pothoulakis C: Clostridium difficile toxin A stimulates macrophage-inflammatory protein-2 production in rat intestinal epithelial cells. J Immunol 160:6039-6045, 1998
26. Castagliuolo I, LaMont JT, Letourneau R, Kelly C, O'Keane JC, Jaffer A, Theoharides TC, Pothoulakis C: Neuronal involvement in the intestinal effects of Clostridium difficile toxin A and Vibrio cholerae enterotoxin in rat ileum. Gastroenterology 107:657-665, 1994
27. Chang J, Rohwer RG: Clostridium difficile infection in adult hamsters. Lab Anim Sci 41:548-552, 1991
28. Clabots CR, Johnson S, Olson MM, Peterson LR, Gerding DN: Acquisition of Clostridium difficile by hospitalized patients: evidence for colonized new admissions as a source of infection. J Infect Dis 166:561-567, 1992
29. Collins JE, Bergeland ME, Bouley D, Ducommun AL, Francis DH, Yeske P: Diarrhea associated with Clostridium perfringens type A enterotoxin in neonatal pigs. J Vet Diagn Invest 1:351-353, 1989
30. Corthier G, Dubos F, Raibaud P: Modulation of cytotoxin production by Clostridium difficile in the intestinal tracts of gnotobiotic mice inoculated with various human intestinal bacteria. Appl Environ Microbiol 49:250-252, 1985
31. Czuprynski CJ, Johnson WJ, Balish E, Wilkins T: Pseudomembranous colitis in Clostridium difficile-monoassociated rats. Infect Immun 39:1368-1376, 1983
32. Dabard J, Dubos F, Martinet L, Ducluzeau R: Experimental reproduction of neonatal diarrhea in young gnotobiotic hares simultaneously associated with Clostridium difficile and other Clostridium strains. Infect Immun 24:7-11, 1979
33. Delmee M: Laboratory diagnosis of Clostridium difficile disease. Clin Microbiol Infect 7:411-416, 2001
34. Dillon ST, Rubin EJ, Yakubovich M, Pothoulakis C, LaMont JT, Feig LA, Gilbert RJ: Involvement of Ras-related Rho proteins in the mechanisms of action of Clostridium difficile toxin A and toxin B. Infect Immun 63:1421-1426, 1995
35. Eglow R, Pothoulakis C, Itzkowitz S, Israel EJ, O'Keane CJ, Gong D, Gao N, Xu YL, Walker WA, LaMont JT: Diminished Clostridium difficile toxin A sensitivity in newborn rabbit ileum is associated with decreased toxin A receptor. J Clin Invest 90:822-829, 1992
36. Eustis SL, Bergeland ME: Suppurative abomasitis associated with Clostridium septicum infection. J Am Vet Med Assoc 178:732-734, 1981
37. Fedorko DP, Williams EC: Use of cycloserine-cefoxitin-fructose agar and L-proline-aminopeptidase (PRO Discs) in the rapid identification of Clostridium difficile. J Clin Microbiol 35:1258-1259, 1997
38. Finegold SM, Attebery HR, Sutter VL: Effect of diet on human fecal flora: comparison of Japanese and American diets. Am J Clin Nutr 27:1456-1469, 1974
39. Finnie JW: Pathogenesis of brain damage produced in sheep by Clostridium perfringens type D epsilon toxin: a review. Aust Vet J 81:219-221, 2003
40. Flegel WA, Muller F, Daubener W, Fischer HG, Hadding U, Northoff H: Cytokine response by human monocytes to Clostridium difficile toxin A and toxin B. Infect Immun 59:3659-3666, 1991
41. Floch MH, Binder HJ, Filburn B, Gershengoren W: The effect of bile acids on intestinal microflora. Am J Clin Nutr 25:1418-1426, 1972
42. Frazier KS, Herron AJ, Hines ME 2nd, Gaskin JM, Altman NH: Diagnosis of enteritis and enterotoxemia due to Clostridium difficile in captive ostriches (Struthio camelus). J Vet Diagn Invest 5:623-625, 1993
43. Freter R: The fatal enteric cholera infection in the guinea pig, achieved by inhibition of normal enteric flora. J Infect Dis 97:57-65, 1955
44. Frisch C, Gerhard R, Aktories K, Hofmann F, Just I: The complete receptor-binding domain of Clostridium difficile toxin A is required for endocytosis. Biochem Biophys Res Commun 300:706-711, 2003
45. Gelev I: [An aerobic bacterium as the causative agent of braxy of sheep]. Zentralbl Bakteriol [Orig] 194:222-235, 1964
46. Genth H, Aktories K, Just I: Monoglucosylation of RhoA at threonine 37 blocks cytosol-membrane cycling. J Biol Chem 274:29050-29056, 1999
47. George WL, Sutter VL, Citron D, Finegold SM: Selective and differential medium for isolation of Clostridium difficile. J Clin Microbiol 9:214-219, 1979
48. Germann PG, Kohler M, Ernst H, Baumgart H, Mohr U: The relation of amyloidosis to social stress induced by crowding in the Syrian hamster (Mesocricetus auratus). Z Versuchstierkd 33:271-275, 1990
49. Gibson GR, Roberfroid MB: Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401-1412, 1995
50. Godec MS: LVG Syrian hamsters developed a syndrome of chronic enteritis associated with Clostridium difficile infection. Lab Anim Sci 42:4, 1992
51. Goncalves C, Decre D, Barbut F, Burghoffer B, Petit JC: Prevalence and characterization of a binary toxin (actin-specific ADP-ribosyltransferase) from Clostridium difficile. J Clin Microbiol 42:1933-1939, 2004
52. Gulke I, Pfeifer G, Liese J, Fritz M, Hofmann F, Aktories K, Barth H: Characterization of the enzymatic component of the ADP-ribosyltransferase toxin CDTa from Clostridium difficile. Infect Immun 69:6004-6011, 2001
53. Gumerlock PH, Tang YJ, Weiss JB, Silva J Jr: Specific detection of toxigenic strains of Clostridium difficile in stool specimens. J Clin Microbiol 31:507-511, 1993
54. Gustafsson A, Baverud V, Gunnarsson A, Rantzien MH, Lindholm A, Franklin A: The association of erythromycin ethylsuccinate with acute colitis in horses in Sweden. Equine Vet J 29:314-318, 1997
55. Hall IC, O'Toole E: Intestinal flora in newborn infants with a description of a new pathogenic anaerobe, Bacillus difficilis. Am J Dis Child 49:390-402, 1935
56. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K: Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56:559-564, 1994
57. Haralambie E, Schmidt-Weinmar A: Infections after experimental cadaver bone marrow transplantation in beagle dogs. Transplantations with and without selective gastrointestinal decontamination. Infection 16:36-41, 1988
58. Harris IE, Portas BH: Enterotoxaemia in rabbits caused by Clostridium spiroforme. Aust Vet J 62:342-343, 1985
59. Hatheway CL: Toxigenic clostridia. Clin Microbiol Rev 3:66-98, 1990
60. He D, Hagen SJ, Pothoulakis C, Chen M, Medina ND, Warny M, LaMont JT: Clostridium difficile toxin A causes early damage to mitochondria in cultured cells. Gastroenterology 119:139-150, 2000
61. He D, Sougioultzis S, Hagen S, Liu J, Keates S, Keates AC, Pothoulakis C, Lamont JT: Clostridium difficile toxin A triggers human colonocyte IL-8 release via mitochondrial oxygen radical generation. Gastroenterology 122:1048-1057, 2002
62. Henriques B, Florin I, Thelestam M: Cellular internalisation of Clostridium difficile toxin A. Microb Pathog 2:455-463, 1987
63. Hofmann F, Busch C, Prepens U, Just I, Aktories K: Localization of the glucosyltransferase activity of Clostridium difficile toxin B to the N-terminal part of the holotoxin. J Biol Chem 272:11074-11078, 1997
64. Hundsberger T, Braun V, Weidmann M, Leukel P, Sauerborn M, von Eichel-Streiber C: Transcription analysis of the genes tcdA-E of the pathogenicity locus of Clostridium difficile. Eur J Biochem 244:735-742, 1997
65. Hurley BW, Nguyen CC: The spectrum of pseudomembranous enterocolitis and antibiotic-associated diarrhea. Arch Intern Med 162:2177-2184, 2002
66. Jobe BA, Grasley A, Deveney KE, Deveney CW, Sheppard BC: Clostridium difficile colitis: an increasing hospital-acquired illness. Am J Surg 169:480-483, 1995
67. Johnson S, Clabots CR, Linn FV, Olson MM, Peterson LR, Gerding DN: Nosocomial Clostridium difficile colonisation and disease. Lancet 336:97-100, 1990
68. Johnson S, Gerding DN, Olson MM, Weiler MD, Hughes RA, Clabots CR, Peterson LR: Prospective, controlled study of vinyl glove use to interrupt Clostridium difficile nosocomial transmission. Am J Med 88:137-140, 1990
69. Jones MA, Hunter D: Isolation of Clostridium difficile from pigs. Vet Rec 112:253, 1983
70. Jones RL, Adney WS, Alexander AF, Shideler RK, Traub-Dargatz JL: Hemorrhagic necrotizing enterocolitis associated with Clostridium difficile infection in four foals. J Am Vet Med Assoc 193:76-79, 1988
71. Jones RL, Adney WS, Shideler RK: Isolation of Clostridium difficile and detection of cytotoxin in the feces of diarrheic foals in the absence of antimicrobial treatment. J Clin Microbiol 25:1225-1227, 1987
72. Just I, Fritz G, Aktories K, Giry M, Popoff MR, Boquet P, Hegenbarth S, von Eichel-Streiber C: Clostridium difficile toxin B acts on the GTPbinding protein Rho. J Biol Chem 269:10706-10712, 1994
73. Just I, Selzer J, Wilm M, von Eichel-Streiber C, Mann M, Aktories K: Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375:500-503, 1995
74. Just I, Wilm M, Selzer J, Rex G, von Eichel-Streiber C, Mann M, Aktories K: The enterotoxin from Clostridium difficile (ToxA) monoglucosylates the Rho proteins. J Biol Chem 270:13932-13936, 1995
75. Kamaras J, Murrell WG: Intestinal epithelial damage in SIDS babies and its similarity to that caused by bacterial toxins in the rabbit. Pathology 33:197-203, 2001
76. Karjalainen T, Barc MC, Collignon A, Trolle S, Boureau H, Cotte-Laffitte J, Bourlioux P: Cloning of a genetic determinant from Clostridium difficile involved in adherence to tissue culture cells and mucus. Infect Immun 62:4347-4355, 1994
77. Karlsson S, Lindberg A, Norin E, Burman LG, Akerlund T: Toxins, butyric acid, and other shortchain fatty acids are coordinately expressed and down-regulated by cysteine in Clostridium difficile. Infect Immun 68:5881-5888, 2000
78. Katz L, LaMont JT, Trier JS, Sonnenblick EB, Rothman SW, Broitman SA, Rieth S: Experimental clindamycin-associated colitis in rabbits. Evidence of toxin-mediated mucosal damage. Gastroenterology 74:246-252, 1978
79. Kelly CP, Becker S, Linevsky JK, Joshi MA, O'Keane JC, Dickey BF, LaMont JT, Pothoulakis C: Neutrophil recruitment in Clostridium difficile toxin A enteritis in the rabbit. J Clin Invest 93:1257-1265, 1994
80. Kelly CP, LaMont JT: Clostridium difficile infection. Annu Rev Med 49:375-390, 1998
81. Kelly CP, LaMont JT: Treatment of Clostridium difficile diarrhea and colitis. In: Gastrointestinal Pharmacotherapy, ed. Wolfe MM, pp. 199-212. WB. Saunders Co., Philadelphia, PA, 1993
82. Knoop FC: Clindamycin-associated enterocolitis in guinea pigs: evidence for a bacterial toxin. Infect Immun 23:31-33, 1979
83. Krivan HC, Clark GF, Smith DF, Wilkins TD: Cell surface binding site for Clostridium difficile enterotoxin: evidence for a glycoconjugate containing the sequence Gal alpha 1-3Gal beta 1-4GlcNAc. Infect Immun 53:573-581, 1986
84. Larson HE, Price AB, Honour P, Borriello SP: Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet 1:1063-1066, 1978
85. Lima AA, Lyerly DM, Wilkins TD, Innes DJ, Guerrant RL: Effects of Clostridium difficile toxins A and B in rabbit small and large intestine in vivo and on cultured cells in vitro. Infect Immun 56:582-588, 1988
86. Linevsky JK, Pothoulakis C, Keates S, Warny M, Keates AC, Lamont JT, Kelly CP: IL-8 release and neutrophil activation by Clostridium difficile toxin-exposed human monocytes. Am J Physiol 273:G1333-G1340, 1997
87. Lowe BR, Fox JG, Bartlett JG: Clostridium difficile-associated cecitis in guinea pigs exposed to penicillin. Am J Vet Res 41:1277-1279, 1980
88. Lusk RH, Fekety R, Silva J, Browne RA, Ringler DH, Abrams GD: Clindamycin-induced enterocolitis in hamsters. J Infect Dis 137:464-475, 1978
89. Lyerly DM, Neville LM, Evans DT, Fill J, Allen S, Greene W, Sautter R, Hnatuck P, Torpey DJ, Schwalbe R: Multicenter evaluation of the Clostridium difficile TOX A/B TEST. J Clin Microbiol 36:184-190, 1998
90. Lyerly DM, Saum KE, MacDonald DK, Wilkins TD: Effects of Clostridium difficile toxins given intragastrically to animals. Infect Immun 47:349-352, 1985
91. Madewell BR, Bea JK, Kraegel SA, Winthrop M, Tang YJ, Silva J Jr: Clostridium difficile: a survey of fecal carriage in cats in a veterinary medical teaching hospital. J Vet Diagn Invest 11:50-54, 1999
92. Madewell BR, Tang YJ, Jang S, Madigan JE, Hirsh DC, Gumerlock PH, Silva J Jr: Apparent outbreaks of Clostridium difficile-associated diarrhea in horses in a veterinary medical teaching hospital. J Vet Diagn Invest 7:343-346, 1995
93. Magdesian KG, Hirsh DC, Jang SS, Hansen LM, Madigan JE: Characterization of Clostridium difficile isolates from foals with diarrhea: 28 cases (1993-1997). J Am Vet Med Assoc 220:67-73, 2002
94. Mantyh CR, McVey DC, Vigna SR: Extrinsic surgical denervation inhibits Clostridium difficile toxin A-induced enteritis in rats. Neurosci Lett 292:95-98, 2000
95. Mathis JN, Pilkinton L, McMillin DE: Detection and transcription of toxin DNA in a nontoxigenic strain of Clostridium difficile. Curr Microbiol 38:324-328, 1999
96. McCracken VJ, Lorenz RG: The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota. Cell Microbiol 3:1-11, 2001
97. McDonel JL: Clostridium perfringens toxins (type A, B, C, D, E). Pharmacol Ther 10:617-655, 1980
98. McFarland LV, Mulligan ME, Kwok RY, Stamm WE: Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 320:204-210, 1989
99. McVey DC, Vigna SR: The capsaicin VR1 receptor mediates substance P release in toxin A-induced enteritis in rats. Peptides 22:1439-1446, 2001
100. Michelich VJ, Nunez-Montiel O, Schuster GS, Thompson F, Dowell VR Jr: Diet as a coadjuvant for development of antibiotic-associated diarrhea in hamsters (Mesocricetus auratus). Lab Anim Sci 31:259-262, 1981
101. Moxley RA, Duhamel GE: Comparative pathology of bacterial enteric diseases of swine. Adv Exp Med Biol 473:83-101, 1999
102. Mukaida N: Interleukin-8: an expanding universe beyond neutrophil chemotaxis and activation. Int J Hematol 72:391-398, 2000
103. Mullany P, Clayton CL, Pallen MJ, Slone R, al-Saleh A, Tabaqchali S: Genes encoding homologues of three consecutive enzymes in the butyrate/butanol-producing pathway of Clostridium acetobutylicum are clustered on the Clostridium difficile chromosome. FEMS Microbiol Lett 124:61-67, 1994
104. Muller EL, Pitt HA, George WL: Prairie dog model for antimicrobial agent-induced Clostridium difficile diarrhea. Infect Immun 55:198-200, 1987
105. Naaber P, Mikelsaar M: Antibiotic-compromised murine model of Clostridium difficile infection. Microecol Ther 25:201-205, 1995
106. Naaber P, Smidt I, Stsepetova J, Brilene T, Annuk H, Mikelsaar M: Inhibition of Clostridium difficile strains by intestinal Lactobacillus species. J Med Microbiol 53:551-554, 2004
107. Olubunmi PA, Taylor DJ: Clostridium perfringens type A in enteric diseases of pigs. Trop Vet 3:28-33, 1985
108. Orchard JL, Fekety R, Smith JR: Antibiotic-associated colitis due to Clostridium difficile in a Kodiak bear. Am J Vet Res 44:1547-1548, 1983
109. Pearson EG, Hedstrom OR, Sonn R, Wedam J: Hemorrhagic enteritis caused by Clostridium perfringens type C in a foal. J Am Vet Med Assoc 188:1309-1310, 1986
110. Peeters JE, Geeroms R, Carman RJ, Wilkins TD: Significance of Clostridium spiroforme in the enteritis-complex of commercial rabbits. Vet Microbiol 12:25-31, 1986
111. Perelle S, Gibert M, Boquet P, Popoff MR: Characterization of Clostridium perfringens iota-toxin genes and expression in Escherichia coli. Infect Immun 61:5147-5156, 1993
112. Perelle S, Gibert M, Bourlioux P, Corthier G, Popoff MR: Production of a complete binary toxin (actin-specific ADP-ribosyltransferase) by Clostridium difficile CD196. Infect Immun 65:1402-1407, 1997
113. Perkins SE, Fox JG, Taylor NS, Green DL, Lipman NS: Detection of Clostridium difficile toxins from the small intestine and cecum of rabbits with naturally acquired enterotoxemia. Lab Anim Sci 45:379-384, 1995
114. Perrin J, Cosmetatos I, Gallusser A, Lobsiger L, Straub R, Nicolet J: Clostridium difficile associated with typhlocolitis in an adult horse. J Vet Diagn Invest 5:99-101, 1993
115. Pfeifer G, Schirmer J, Leemhuis J, Busch C, Meyer DK, Aktories K, Barth H: Cellular uptake of Clostridium difficile toxin B. Translocation of the N-terminal catalytic domain into the cytosol of eukaryotic cells. J Biol Chem 278:44535-44541, 2003
116. Post KW, Jost BH, Songer JG: Evaluation of a test for Clostridium difficile toxins A and B for the diagnosis of neonatal swine enteritis. J Vet Diagn Invest 14:258-259, 2002
117. Pothoulakis C, Castagliuolo I, LaMont JT, Jaffer A, O'Keane JC, Snider RM, Leeman SE: CP-96,345, a substance P antagonist, inhibits rat intestinal responses to Clostridium difficile toxin A but not cholera toxin. Proc Natl Acad Sci U S A 91:947-951, 1994
118. Pothoulakis C, Gilbert RJ, Cladaras C, Castagliuolo I, Semenza G, Hitti Y, Montcrief JS, Linevsky J, Kelly CP, Nikulasson S, Desai HP, Wilkins TD, LaMont JT: Rabbit sucrase-isomaltase contains a functional intestinal receptor for Clostridium difficile toxin A. J Clin Invest 98:641-649, 1996
119. Pothoulakis C, Lamont JT: Microbes and microbial toxins: paradigms for microbial-mucosal interactions II. The integrated response of the intestine to Clostridium difficile toxins. Am J Physiol Gastrointest Liver Physiol 280:G178-G183, 2001
120. Qa'Dan M, Spyres LM, Ballard JD: pH-induced conformational changes in Clostridium difficile toxin B. Infect Immun 68:2470-2474, 2000
121. Rastall RA: Bacteria in the gut: friends and foes and how to alter the balance. J Nutr 134:2022S-2026S, 2004
122. Ratnaike RN, Jones TE: Mechanisms of druginduced diarrhoea in the elderly. Drugs Aging 13:245-253, 1998
123. Rehg JE, Lu YS: Clostridium difficile typhlitis in hamsters not associated with antibiotic therapy. J Am Vet Med Assoc 181:1422-1423, 1982
124. Riley TV, Adams JE, O'Neill GL, Bowman RA: Gastrointestinal carriage of Clostridium difficile in cats and dogs attending veterinary clinics. Epidemiol Infect 107:659-665, 1991
125. Rolfe RD: Binding kinetics of Clostridium difficile toxins A and B to intestinal brush border membranes from infant and adult hamsters. Infect Immun 59:1223-1230, 1991
126. Rolfe RD: Role of volatile fatty acids in colonization resistance to Clostridium difficile. Infect Immun 45:185-191, 1984
127. Rolfe RD, Iaconis JP: Intestinal colonization of infant hamsters with Clostridium difficile. Infect Immun, 42:480-486. 1983
128. Rolland RM, Chalifoux LV, Snook SS, Ausman LM, Johnson LD: Five spontaneous deaths associated with Clostridium difficile in a colony of cotton-top tamarins (Saguinus oedipus). Lab Anim Sci 47:472-476, 1997
129. Rood JI, Cole ST: Molecular genetics and pathogenesis of Clostridium perfringens. Microbiol Rev 55:621-648, 1991
130. Rubin MS, Bodenstein LE, Kent KC: Severe Clostridium difficile colitis. Dis Colon Rectum 38:350-354, 1995
131. Ryden EB, Lipman NS, Taylor NS, Rose R, Fox JG: Clostridium difficile typhlitis associated with cecal mucosal hyperplasia in Syrian hamsters. Lab Anim Sci 41:553-558, 1991
132. Sambol SP, Tang JK, Merrigan MM, Johnson S, Gerding DN: Infection of hamsters with epidemiologically important strains of Clostridium difficile. J Infect Dis 183:1760-1766, 2001
133. Savage DC: Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107-133, 1977
134. Schirmer J, Aktories K: Large clostridial cytotoxins: cellular biology of Rho/Ras-glucosylating toxins. Biochim Biophys Acta 1673:66-74, 2004
135. Schue V, Green GA,Monteil H: Comparison of the ToxA test with cytotoxicity assay and culture for the detection of Clostridium difficile-associated diarrhoea disease. J Med Microbiol 41:316-318, 1994
136. Shivaprasad HL: Hepatitis associated with Clostridium difficile in an ostrich chick. Avian Pathol 32:57-62, 2003
137. Small JD: Fatal enterocolitis in hamsters given lincomycin hydrochloride. Lab Anim Care 18:411-420, 1968
138. Songer J, Post K, Larson D, Jost B, Glock R: Infection of neonatal swine with Clostridium difficile. Swine Hlth Prod 8:185-189, 2000
139. Songer JG: Clostridial diseases of small ruminants. Vet Res 29:219-232, 1998
140. Songer JG: Clostridial enteric diseases of domestic animals. Clin Microbiol Rev 9:216-234, 1996
141. Sorensson J, Jodal M, Lundgren O: Involvement of nerves and calcium channels in the intestinal response to Clostridium difficile toxin A: an experimental study in rats in vivo. Gut 49:56-65, 2001
142. Struble AL, Tang YJ, Kass PH, Gumerlock PH, Madewell BR, Silva J Jr: Fecal shedding of Clostridium difficile in dogs: a period prevalence survey in a veterinary medical teaching hospital. J Vet Diagn Invest 6:342-347, 1994
143. Su WJ, Waechter MJ, Bourlioux P, Dolegeal M, Fourniat J, Mahuzier G: Role of volatile fatty acids in colonization resistance to Clostridium difficile in gnotobiotic mice. Infect Immun 55:1686-1691, 1987
144. Sullivan NM, Pellett S, Wilkins TD: Purification and characterization of toxins A and B of Clostridium difficile. Infect Immun 35:1032-1040, 1982
145. Tang YJ, Gumerlock PH, Weiss JB, Silva J Jr: Specific detection of Clostridium difficile toxin A gene sequences in clinical isolates. Mol Cell Probes 8:463-467, 1994
146. Taylor NS, Thorne GM, Bartlett JG: Comparison of two toxins produced by Clostridium difficile. Infect Immun 34:1036-1043, 1981
147. Thomas C, Stevenson M, Riley TV: Antibiotics and hospital-acquired Clostridium difficile-associated diarrhoea: a systematic review. J Antimicrob Chemother 51:1339-1350, 2003
148. Traub-Dargatz JL, Jones RL: Clostridia-associated enterocolitis in adult horses and foals. Vet Clin North Am Equine Pract 9:411-421, 1993
149. Triadafilopoulos G, Pothoulakis C, Weiss R, Giampaolo C, Lamont JT: Comparative study of Clostridium difficile toxin A and cholera toxin in rabbit ileum. Gastroenterology 97:1186-1192, 1989
150. Tsai C-C: Clostridia as pathogens for diarrheal diseases in monkeys. Proc Soc Exp Biol Med 185:238, 1986
151. Tucker KD, Wilkins TD: Toxin A of Clostridium difficile binds to the human carbohydrate antigens I, X, and Y. Infect Immun 59:73-78, 1991
152. Uzal FA, Kelly WR, Morris WE, Bermudez J, Baison M: The pathology of peracute experimental Clostridium perfringens type D enterotoxemia in sheep. J Vet Diagn Invest 16:403-411, 2004
153. van den Berg RJ, Claas EC, Oyib DH, Klaassen CH, Dijkshoorn L, Brazier JS, Kuijper EJ: Characterization of toxin A-negative, toxin B-positive Clostridium difficile isolates from outbreaks in different countries by amplified fragment length polymorphism and PCR ribotyping. J Clin Microbiol 42:1035-1041, 2004
154. Viscidi R, Willey S, Bartlett JG: Isolation rates and toxigenic potential of Clostridium difficile isolates from various patient populations. Gastroenterology 81:5-9, 1981
155. von Eichel-Streiber C, Laufenberg-Feldmann R, Sartingen S, Schulze J, Sauerborn M: Comparative sequence analysis of the Clostridium difficile toxins A and B. Mol Gen Genet 233:260-268, 1992
156. Waters EH, Orr JP, Clark EG, Schaufele CM: Typhlocolitis caused by Clostridium difficile in suckling piglets. J Vet Diagn Invest 10:104-108, 1998
157. Weese JS, Parsons DA, Staempfli HR: Association of Clostridium difficile with enterocolitis and lactose intolerance in a foal. J Am Vet Med Assoc 214:229-232, 205, 1999
158. Weese JS, Staempfli HR, Prescott JF: Isolation of environmental Clostridium difficile from a veterinary teaching hospital. J Vet Diagn Invest 12:449-452, 2000
159. Weese JS, Staempfli HR, Prescott JF: A prospective study of the roles of Clostridium difficile and enterotoxigenic Clostridium perfringens in equine diarrhoea. Equine Vet J 33:403-409, 2001
160. Weese JS, Staempfli HR, Prescott JF: Survival of Clostridium difficile and its toxins in equine feces: implications for diagnostic test selection and interpretation. J Vet Diagn Invest 12:332-336, 2000
161. Weese JS, Staempfli HR, Prescott JF, Kruth SA, Greenwood SJ, Weese HE: The roles of Clostridium difficile and enterotoxigenic Clostridium perfringens in diarrhea in dogs. J Vet Intern Med 15:374-378, 2001
162. Weese JS, Weese HE, Bourdeau TL, Staempfli HR: Suspected Clostridium difficile-associated diarrhea in two cats. J Am Vet Med Assoc 218:1436-1439, 1421, 2001
163. Wershil BK, Castagliuolo I, Pothoulakis C: Direct evidence of mast cell involvement in Clostridium difficile toxin A-induced enteritis in mice. Gastroenterology 114:956-964, 1998
164. Wilson KH: The microecology of Clostridium difficile. Clin Infect Dis 16 (Suppl 4): S214-S218, 1993
165. Wilson KH, Kennedy MJ, Fekety FR: Use of sodium taurocholate to enhance spore recovery on a medium selective for Clostridium difficile. J Clin Microbiol 15:443-446, 1982
166. Wilson KH, Perini F: Role of competition for nutrients in suppression of Clostridium difficile by the colonic microflora. Infect Immun 56:2610-2614, 1988
167. Wilson KH, Sheagren JN, Freter R: Population dynamics of ingested Clostridium difficile in the gastrointestinal tract of the Syrian hamster. J Infect Dis 151:355-361, 1985
168. Wilson KH, Silva J, Fekety FR: Suppression of Clostridium difficile by normal hamster cecal flora and prevention of antibiotic-associated cecitis. Infect Immun 34:626-628, 1981
169. Xia Y, Hu HZ, Liu S, Pothoulakis C, Wood JD: Clostridium difficile toxin A excites enteric neurones and suppresses sympathetic neurotransmission in the guinea pig. Gut 46:481-486, 2000
170. Zhong SS, Zhang ZS, Wang JD, Lai ZS, Wang QY, Pan LJ, Ren YX: Competitive inhibition of adherence of enterotoxigenic Escherichia coli, enteropathogenic Escherichia coli and Clostridium difficile to intestinal epithelial cell line Lovo by purified adhesin of Bifidobacterium adolescentis 1027. World J Gastroenterol 10:1630-1633, 2004