Establishment of an endogenous Clostridium difficile rat infection model and evaluation of the effects of Clostridium butyricum MIYAIRI 588 probiotic strain

Frontiers in Microbiology

Volumn 9, Issue JUN, 2018, Pages

  Oka, Kentaro ^a   Osaki, Takako ^b   Hanawa, Tomoko ^b   Kurata, Satoshi ^b   Sugiyama, Emi ^a   Takahashi, Motomichi ^a,b   Tanaka, Mamoru ^a   Taguchi, Haruhiko ^c   Kamiya, Shigeru ^b  

^a Miyarisan Pharmaceutical Co   (Japan)

^b KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c KYORIN UNIVERSITY   (Japan)

Author keywords

C. difficile associated diarrhea; C. difficile infection model; Clostridium butyricum; Clostridium difficile; Probiotics

Indexed keywords

BIOTIN; CLINDAMYCIN PHOSPHATE; CYTOTOXIN; DALACIN S; METRONIDAZOLE; PROBIOTIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; BACTEROIDES; CLOSTRIDIUM BUTYRICUM; CLOSTRIDIUM DIFFICILE INFECTION; CYTOTOXICITY ASSAY; DIARRHEA; EXPERIMENTAL INFECTION; FECAL WATER CONTENT; FECES ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; RAT; RIBOTYPING; SYRIAN HAMSTER;

EID: 85048617972     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.01264     Document Type: Article

References (42)

1. al Saif, N., and Brazier, J. S. (1996). The distribution of Clostridium difficile in the environment of South Wales. J. Med. Microbiol. 45, 133-137. doi: 10.1099/00222615-45-2-133
2. Anton, P. M., O'Brien, M., Kokkotou, E., Eisenstein, B., Michaelis, A., Rothstein, D., et al. (2004). Rifalazil treats and prevents relapse of Clostridium difficile-associated diarrhea in hamsters. Antimicrob. Agents Chemother. 48, 3975-3979. doi: 10.1128/AAC.48.10.3975-3979.2004
3. Aronsson, B., Möllby, R., and Nord, C. E. (1985). Antimicrobial agents and Clostridium difficile in acute enteric disease: epidemiological data from Sweden, 1980-1982. J. Infect. Dis. 151, 476-481. doi: 10.1093/infdis/151.3.476
4. Bartlett, J. G., Chang, T. W., Gurwith, M., Gorbach, S. L., and Onderdonk, A. B. (1978). Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N. Engl. J. Med. 298, 531-534. doi: 10.1056/NEJM197803092981003
5. Chen, S., Sun, C., Wang, H., and Wang, J. (2015). The role of Rho GTPases in toxicity of Clostridium difficile toxins. Toxins 7, 5254-5267. doi: 10.3390/toxins7124874
6. Chen, X., Katchar, K., Goldsmith, J. D., Nanthakumar, N., Cheknis, A., Gerding, D. N., et al. (2008). A mouse model of Clostridium difficile-associated disease. Gastroenterology 135, 1984-1992. doi: 10.1053/j.gastro.2008.09.002
7. Drudy, D., Fanning, S., and Kyne, L. (2007). Toxin A-negative, toxin B-positive Clostridium difficile. Int. J. Infect. Dis. 11, 5-10. doi: 10.1016/j.ijid.2006.04.003
8. Eglow, R., Pothoulakis, C., Itzkowitz, S., Israel, E. J., O'Keane, C. J., Gong, D., et al. (1992). Diminished Clostridium difficile toxin A sensitivity in newborn rabbit ileum is associated with decreased toxin A receptor. J. Clin. Invest. 90, 822-829. doi: 10.1172/JCI115957
9. Finegold, S. M., Sutter, V. L., and Mathisen, G. E. (1983). "Normal indigenous intestinal flora," in Human Intestinal Microflora in Health and Disease, ed. D. J. Hentges (New York, NY: Academic Press), 3-31. doi: 10.1016/B978-0-12-341280-5.50007-0
10. Gumerlock, P. H., Tang, Y. J., Meyers, F. J., and Silva, J. Jr. (1991). Use of the polymerase chain reaction for the specific and direct detection of Clostridium difficile in human feces. Rev. Infect. Dis. 13, 1053-1060. doi: 10.1093/clinids/13.6.1053
11. Hayashi, A., Sato, T., Kamada, N., Mikami, Y., Matsuoka, K., Hisamatsu, T., et al. (2013). A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host Microbe 13, 711-722. doi: 10.1016/j.chom.2013.05.013
12. Janezic, S., Zidaric, V., Pardon, B., Indra, A., Kokotovic, B., Blanco, J. L., et al. (2014). International Clostridium difficile animal strain collection and large diversity of animal associated strains. BMC Microbiol. 14:173. doi: 10.1186/1471-2180-14-173
13. Jonsson, E., and Conway, P. (1992). "Probiotics for pigs," in Probiotics, the Scientific Basis, ed. R. Fuller (London: Chapman and Hall), 259-316
14. Kamiya, S., and Borriello, S. P. (1992). A non-haemagglutinating form of Clostridium difficile toxin A. J. Med. Microbiol. 36, 190-197. doi: 10.1099/00222615-36-3-190
15. Kamiya, S., Taguchi, H., Yamaguchi, H., Osaki, T., Takahashi, M., and Nakamura, S. (1997). Bacterioprophylaxis using Clostridium butyricum for lethal caecitis by Clostridium difficile in gnotobiotic mice. Rev. Med. Microbiol. 8(Suppl.1), S57-S59. doi: 10.1097/00013542-199712001-00029
16. Kato, H., Kato, N., Watanabe, K., Iwai, N., Nakamura, H., Yamamoto, T., et al. (1998). Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. J. Clin. Microbiol. 36, 2178-2182
17. Kato, H., Kato, N., Watanabe, K., Ueno, K., Ushijima, H., Hashira, S., et al. (1994). Application of typing by pulsed-field gel electrophoresis to the study of Clostridium difficile in a neonatal intensive care unit. J. Clin. Microbiol. 32, 2067-2070
18. Kato, H., Kita, H., Karasawa, T., Maegawa, T., Koino, Y., Takakuwa, H., et al. (2001). Colonisation and transmission of Clostridium difficile in healthy individuals examined by PCR ribotyping and pulsed-field gel electrophoresis. J. Med. Microbiol. 50, 720-727. doi: 10.1099/0022-1317-50-8-720
19. Kato, N., Ou, C. Y., Kato, H., Bartley, S. L., Brown, V. K., Dowell, V. R. Jr., et al. (1991). Identification of toxigenic Clostridium difficile by the polymerase chain reaction. J. Clin. Microbiol. 29, 33-37
20. Keel, M. K., and Songer, J. G. (2007). The distribution and density of Clostridium difficile toxin receptors on the intestinal mucosa of neonatal pigs. Vet. Pathol. 44, 814-822. doi: 10.1354/vp.44-6-814
21. Kelly, C. P., and LaMont, J. T. (2008). Clostridium difficile-more difficult than ever. N. Engl. J. Med. 359, 1932-1940. doi: 10.1056/NEJMra0707500
22. Kelly, C. P., Pothoulakis, C., and LaMont, J. T. (1994). Clostridium difficile colitis. N. Engl. J. Med. 330, 257-262. doi: 10.1056/NEJM199401273300406
23. Kink, J. A., and Williams, J. A. (1998). Antibodies to recombinant Clostridium difficile toxins A and B are an effective treatment and prevent relapse of C. difficile-associated disease in a hamster model of infection. Infect. Immun. 66, 2018-2025
24. Kuehne, S. A., Cartman, S. T., Heap, J. T., Kelly, M. L., Cockayne, A., and Minton, N. P. (2010). The role of toxin A and toxin B in Clostridium difficile infection. Nature 467, 711-713. doi: 10.1038/nature09397
25. Kurita, A., Kado, S., Kaneda, N., Onoue, M., Hashimoto, S., and Yokokura, T. (2000). Modified irinotecan hydrochloride (CPT-11) administration schedule improves induction of delayed-onset diarrhea in rats. Cancer Chemother. Pharmacol. 46, 211-220. doi: 10.1007/s002800000151
26. Löfmark, S., Edlund, C., and Nord, C. E. (2010). Metronidazole is still the drug of choice for treatment of anaerobic infections. Clin. Infect. Dis. 50(Suppl.1), S16-S23. doi: 10.1086/647939
27. Lyras, D., O'Connor, J. R., Howarth, P. M., Sambol, S. P., Carter, G. P., Phumoonna, T., et al. (2009). Toxin B is essential for virulence of Clostridium difficile. Nature 458, 1176-1179. doi: 10.1038/nature07822
28. Mitsuoka, T. (1978). Intestinal Bacteria and Health. Tokyo: Harcourt Brace Jovanovich Japan
29. Nakamura, S., Mikawa, M., Nakashio, S., Takabatake, M., Okado, I., Yamakawa, K., et al. (1981). Isolation of Clostridium difficile from the feces and the antibody in sera of young and elderly adults. Microbiol. Immunol. 25, 345-351. doi: 10.1111/j.1348-0421.1981.tb00036.x
30. Nakanishi, S., Kataoka, K., Kuwahara, T., and Ohnishi, Y. (2003). Effects of high amylose maize starch and Clostridium butyricum on metabolism in colonic microbiota and formation of azoxymethane-induced aberrant crypt foci in the rat colon. Microbiol. Immunol. 47, 951-958. doi: 10.1111/j.1348-0421.2003.tb03469.x
31. Oka, K., Osaki, T., Hanawa, T., Kurata, S., Okazaki, M., Manzoku, T., et al. (2012). Molecular and microbiological characterization of Clostridium difficile isolates from single, relapse, and reinfection cases. J. Clin. Microbiol. 50, 915-921. doi: 10.1128/JCM.0558811
32. Rupnik, M., Wilcox, M. H., and Gerding, D. N. (2009). Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7, 526-536. doi: 10.1038/nrmicro2164
33. Sambol, S. P., Tang, J. K., Merrigan, M. M., Johnson, S., and Gerding, D. N. (2001). Infection of hamsters with epidemiologically important strains of Clostridium difficile. J. Infect. Dis. 183, 1760-1766. doi: 10.1086/320736
34. Sato, R., and Tanaka, M. (1997). Intestinal distribution and intraluminal localization of orally administered Clostridium butyricum in rats. Microbiol. Immunol. 41, 665-671. doi: 10.1111/j.1348-0421.1997.tb01909.x
35. Seki, H., Shiohara, M., Matsumura, T., Miyagawa, N., Tanaka, M., Komiyama, A., et al. (2003). Prevention of antibiotic-associated diarrhea in children by Clostridium butyricum MIYAIRI. Pediatr. Int. 45, 86-90. doi: 10.1046/j.1442-200X.2003.01671.x
36. Swanson, R. N., Hardy, D. J., Shipkowitz, N. L., Hanson, C. W., Ramer, N. C., Fernandes, P. B., et al. (1991). In vitro and in vivo evaluation of tiacumicins B and C against Clostridium difficile. Antimicrob. Agents Chemother. 35, 1108-1111. doi: 10.1128/AAC.35.6.1108
37. Takahashi, M., Taguchi, H., Yamaguchi, H., Osaki, T., and Kamiya, S. (2000). Studies of the effect of Clostridium butyricum on Helicobacter pylori in several test models including gnotobiotic mice. J. Med. Microbiol. 49, 635-642. doi: 10.1099/0022-1317-49-7-635
38. Takahashi, M., Taguchi, H., Yamaguchi, H., Osaki, T., Komatsu, A., and Kamiya, S. (2004). The effect of probiotic treatment with Clostridium butyricum on enterohemorrhagic Escherichia coli O157:H7 infection in mice. FEMS Immunol. Med. Microbiol. 41, 219-226. doi: 10.1016/j.femsim.2004.03.010
39. Usui, M., Nanbu, Y., Oka, K., Takahashi, M., Inamatsu, T., Asai, T., et al. (2014). Genetic relatedness between Japanese and European isolates of Clostridium difficile originating from piglets and their risk associated with human health. Front. Microbiol. 5:513. doi: 10.3389/fmicb.2014.00513
40. Viscidi, R., Willey, S., and Bartlett, J. G. (1981). Isolation rates and toxigenic potential of Clostridium difficile isolates from various patient populations. Gastroenterology 81, 5-9
41. Woo, T. D., Oka, K., Takahashi, M., Hojo, F., Osaki, T., Hanawa, T., et al. (2011). Inhibition of the cytotoxic effect of Clostridium difficile in vitro by Clostridium butyricum MIYAIRI 588 strain. J. Med. Microbiol. 60(Pt 11), 1617-1625. doi: 10.1099/jmm.0.033423-0
42. Yamakawa, K., Karasawa, T., Ikoma, S., and Nakamura, S. (1996). Enhancement of Clostridium difficile toxin production in biotin-limited conditions. J. Med. Microbiol. 44, 111-114. doi: 10.1099/00222615-44-2-111