Small animal models for the study of Clostridium difficile disease pathogenesis

FEMS Microbiology Letters

Volumn 352, Issue 2, 2014, Pages 140-149

  Hutton, Melanie L ^a   Mackin, Kate E ^a   Chakravorty, Anjana ^a   Lyras, Dena ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Animal model; Clostridium difficile; Diarrhoea; Hamster; Mouse; Toxin

Indexed keywords

CEFOPERAZONE; CLINDAMYCIN; COLISTIN; GENTAMICIN; KANAMYCIN; METRONIDAZOLE; VANCOMYCIN;

ANIMAL MODEL; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; DEVELOPED COUNTRY; DIARRHEA; DISEASE MODEL; GNOTOBIOTICS; HAMSTER MODEL; HUMAN; INNATE IMMUNITY; MOUSE MODEL; NONHUMAN; PATHOGENESIS; PORCINE MODEL; PRIORITY JOURNAL; REVIEW;

ANIMALIA; BACTERIA (MICROORGANISMS); CLOSTRIDIUM DIFFICILE; CRICETINAE; SUIDAE;

ANIMAL MODEL; CLOSTRIDIUM DIFFICILE; DIARRHOEA; HAMSTER; MOUSE; TOXIN;

ANIMALS; ANTI-BACTERIAL AGENTS; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; CRICETINAE; DIARRHEA; DISEASE MODELS, ANIMAL; HUMANS; MICE; SWINE;

EID: 84897028931     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12367     Document Type: Review

References (51)

1. Bartlett JG, Onderdonk AB & Cisneros RL (1977a) Clindamycin-associated colitis in hamsters: protection with vancomycin. Gastroenterology 73: 772-776.
2. Bartlett JG, Onderdonk AB, Cisneros RL & Kasper DL (1977b) Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters. J Infect Dis 136: 701-705.
3. Bartlett JG, Chang TW, Moon N & Onderdonk AB (1978a) 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.
4. Bartlett JG, Moon N, Chang TW, Taylor N & Onderdonk AB (1978b) Role of Clostridium difficile in antibiotic-associated pseudomembranous colitis. Gastroenterology 75: 778-782.
5. Bartlett JG, Chang TW, Gurwith M, Gorbach SL & Onderdonk AB (1978c) Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med 298: 531-534.
6. Best EL, Freeman J & Wilcox MH (2012) Models for the study of Clostridium difficile infection. Gut Microbes 3: 145-167.
7. Borriello SP & Barclay FE (1985) Protection of hamsters against Clostridium difficile ileocaecitis by prior colonisation with non-pathogenic strains. J Med Microbiol 19: 339-350.
8. Borriello SP, Ketley JM, Mitchell TJ, Barclay FE, Welch AR, Price AB & Stephen J (1987) Clostridium difficile-a spectrum of virulence and analysis of putative virulence determinants in the hamster model of antibiotic-associated colitis. J Med Microbiol 24: 53-64.
9. Buckley AM, Spencer J, Candlish D, Irvine JJ & Douce GR (2011) Infection of hamsters with the UK Clostridium difficile ribotype 027 outbreak strain R20291. J Med Microbiol 60: 1174-1180.
10. Buckley AM, Spencer J, Maclellan LM, Candlish D, Irvine JJ & Douce GR (2013) Susceptibility of hamsters to Clostridium difficile isolates of differing toxinotype. PLoS One 8: e64121.
11. Buffie CG, Jarchum I, Equinda M et al. (2012) Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect Immun 80: 62-73.
12. Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, Gerding DN & Kelly CP (2008) A mouse model of Clostridium difficile-associated disease. Gastroenterology 135: 1984-1992.
13. Deakin LJ, Clare S, Fagan RP et al. (2012) The Clostridium difficile spo0A gene is a persistence and transmission factor. Infect Immun 80: 2704-2711.
14. Delmee M & Avesani V (1990) Virulence of ten serogroups of Clostridium difficile in hamsters. J Med Microbiol 33: 85-90.
15. George RH, Symonds JM, Dimock F et al. (1978) Identification of Clostridium difficile as a cause of pseudomembranous colitis. Br Med J 1: 695.
16. Gerding DN (2004) Clindamycin, cephalosporins, fluoroquinolones, and Clostridium difficile-associated diarrhea: this is an antimicrobial resistance problem. Clin Infect Dis 38: 646-648.
17. Goulding D, Thompson H, Emerson J, Fairweather NF, Dougan G & Douce GR (2009) Distinctive profiles of infection and pathology in hamsters infected with Clostridium difficile strains 630 and B1. Infect Immun 77: 5478-5485.
18. Hamm EE, Voth DE & Ballard JD (2006) Identification of Clostridium difficile toxin B cardiotoxicity using a zebrafish embryo model of intoxication. P Natl Acad Sci USA 103: 14176-14181.
19. Hirota SA, Iablokov V, Tulk SE et al. (2012) Intrarectal instillation of Clostridium difficile toxin A triggers colonic inflammation and tissue damage: development of a novel and efficient mouse model of Clostridium difficile toxin exposure. Infect Immun 80: 4474-4484.
20. Ivanov II, Frutos Rde L, Manel N et al. (2008) Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4: 337-349.
21. Jank T & Aktories K (2008) Structure and mode of action of clostridial glucosylating toxins: the ABCD model. Trends Microbiol 16: 222-229.
22. Janoir C, Deneve C, Bouttier S et al. (2013) Adaptive strategies and pathogenesis of Clostridium difficile from in vivo transcriptomics. Infect Immun 81: 3757-3769.
23. Johnson S (2012) Meeting the challenge of recurrent Clostridium difficile infection. J Hosp Med 7(Suppl 3): S11-S13.
24. Johnson S, Samore MH, Farrow KA et al. (1999) Epidemics of diarrhea caused by a clindamycin-resistant strain of Clostridium difficile in four hospitals. N Engl J Med 341: 1645-1651.
25. Keel MK & Songer JG (2006) The comparative pathology of Clostridium difficile-associated disease. Vet Pathol 43: 225-240.
26. Kelly CP & LaMont JT (2008) Clostridium difficile - more difficult than ever. N Engl J Med 359: 1932-1940.
27. Kuehne SA, Cartman ST, Heap JT, Kelly ML, Cockayne A & Minton NP (2010) The role of toxin A and toxin B in Clostridium difficile infection. Nature 467: 711-713.
28. Kuehne SA, Collery MM, Kelly ML, Cartman ST, Cockayne A & Minton NP (2014) The importance of toxin A, toxin B and CDT in virulence of an epidemic Clostridium difficile strain. J Infect Dis 209: 83-86.
29. Lanis JM, Barua S & Ballard JD (2010) Variations in TcdB activity and the hypervirulence of emerging strains of Clostridium difficile. PLoS Pathog 6: e1001061.
30. Larson HE & Borriello SP (1990) Quantitative study of antibiotic-induced susceptibility to Clostridium difficile enterocecitis in hamsters. Antimicrob Agents Chemother 34: 1348-1353.
31. Larson HE, Price AB & Borriello SP (1980) Epidemiology of experimental enterocecitis due to Clostridium difficile. J Infect Dis 142: 408-413.
32. Lawley TD & Young VB (2013) Murine models to study Clostridium difficile infection and transmission. Anaerobe 24: 94-97.
33. Lawley TD, Clare S, Walker AW et al. (2009) Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect Immun 77: 3661-3669.
34. Lawley TD, Clare S, Walker AW et al. (2012) Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLoS Pathog 8: e1002995.
35. Libby JM, Jortner BS & Wilkins TD (1982) Effects of the two toxins of Clostridium difficile in antibiotic-associated cecitis in hamsters. Infect Immun 36: 822-829.
36. Lyerly DM, Saum KE, MacDonald DK & Wilkins TD (1985) Effects of Clostridium difficile toxins given intragastrically to animals. Infect Immun 47: 349-352.
37. Lyras D, O'Connor JR, Howarth PM et al. (2009) Toxin B is essential for virulence of Clostridium difficile. Nature 458: 1176-1179.
38. Macpherson AJ & Harris NL (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4: 478-485.
39. Pawlowski SW, Calabrese G, Kolling GL et al. (2010) Murine model of Clostridium difficile infection with aged gnotobiotic C57BL/6 mice and a BI/NAP1 strain. J Infect Dis 202: 1708-1712.
40. Price A, Larson H & Crow J (1979) Morphology of experimental antibiotic-associated enterocolitis in the hamster: a model for human pseudomembranous colitis and antibiotic-associated diarrhoea. Gut 20: 467-475.
41. Razaq N, Sambol S, Nagaro K, Zukowski W, Cheknis A, Johnson S & Gerding DN (2007) Infection of hamsters with historical and epidemic BI types of Clostridium difficile. J Infect Dis 196: 1813-1819.
42. Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD & Young VB (2011) The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile Infection. Gut Microbes 2: 145-158.
43. Reeves AE, Koenigsknecht MJ, Bergin IL & Young VB (2012) Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect Immun 80: 3786-3794.
44. Sambol SP, Tang JK, Merrigan MM, Johnson S & Gerding DN (2001) Infection of hamsters with epidemiologically important strains of Clostridium difficile. J Infect Dis 183: 1760-1766.
45. Small JD (1968) Fatal enterocolitis in hamsters given lincomycin hydrochloride. Lab Anim Care 18: 411-420.
46. Steiner TS, Flores CA, Pizarro TT & Guerrant RL (1997) Fecal lactoferrin, interleukin-1beta, and interleukin-8 are elevated in patients with severe Clostridium difficile colitis. Clin Diagn Lab Immunol 4: 719-722.
47. Sullivan A, Edlund C & Nord CE (2001) Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis 1: 101-114.
48. Sun X, Wang H, Zhang Y, Chen K, Davis B & Feng H (2011) Mouse relapse model of Clostridium difficile infection. Infect Immun 79: 2856-2864.
49. Theriot CM, Koumpouras CC, Carlson PE, Bergin II, Aronoff DM & Young VB (2011) Cefoperazone-treated mice as an experimental platform to assess differential virulence of Clostridium difficile strains. Gut Microbes 2: 326-334.
50. Voth DE & Ballard JD (2005) Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev 18: 247-263.
51. Wilson KH & Sheagren JN (1983) Antagonism of toxigenic Clostridium difficile by nontoxigenic C. difficile. J Infect Dis 147: 733-736.