Hostname: page-component-7c8c6479df-94d59 Total loading time: 0 Render date: 2024-03-28T19:17:49.442Z Has data issue: false hasContentIssue false

Protective effect of bifidobacteria in an experimental model of Clostridium difficile associated colitis

Published online by Cambridge University Press:  23 April 2013

Fernando M. Trejo
Affiliation:
CCT La Plata – CONICET – Centro de Investigación y Desarrollo en Criotecnología de Alimentos (CIDCA), Facultad de Ciencias Exactas, Universidad Nacional de La Plata, 47 y 116, La Plata 1900, Argentina
Graciela L. De Antoni
Affiliation:
Cátedra de Microbiología, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, 47 y 116, La Plata 1900, Argentina CIC-PBA-Comisión de Invetigaciones Cientificas de la Provincia de Buenos Aires, Argentina
Pablo F. Pérez*
Affiliation:
CCT La Plata – CONICET – Centro de Investigación y Desarrollo en Criotecnología de Alimentos (CIDCA), Facultad de Ciencias Exactas, Universidad Nacional de La Plata, 47 y 116, La Plata 1900, Argentina Cátedra de Microbiología, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, 47 y 116, La Plata 1900, Argentina
*
*For correspondence; e-mail: pfp@biol.unlp.edu.ar

Abstract

The aim of this study was to evaluate the ability of Bifidobacterium strains to prevent the effects associated with Clostridium difficile infection in a hamster model of enterocolitis. After clindamycin treatment (30 mg/kg), animals were infected intragastrically with C. difficile (5×108 CFU per animal). Seven days prior to antibiotic administration, probiotic treatment was started by administering bacterial suspensions of bifidobacteria in drinking water. Strains CIDCA 531, CIDCA 5310, CIDCA 5316, CIDCA 5320, CIDCA 5323 and CIDCA 5325 were used. Treatment was continued during all the experimental period. Development of diarrhoea, enterocolitis and mortality were evaluated. All the infected animals belonging to the placebo group developed enterocolitis (5/5) and only two dead (2/5) whereas in the group administered with Bifidobacterium bifidum strain CIDCA 5310 the ratio of animals with enterocolitis or dead decreased significantly (1/5 and 0/5 respectively). Biological activity of caecum contents was evaluated in vitro on Vero cells. Animals treated with strain CIDCA 5310 presented lower biological activity than those belonging to the placebo group. The present study shows the potential of selected strains of bifidobacteria to antagonise, in vivo, the virulence of C. difficile.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2013 

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

Arroyo, LG, Kruth, SA, Willey, BM, Staempfli, HR, Low, DE & Weese, JS 2005 PCR ribotyping of Clostridium difficile isolates originating from human and animal sources. Journal of Medical Microbiology 54 163166Google Scholar
Aslam, S, Hamill, RJ & Musher, DM 2005 Treatment of Clostridium difficile-associated disease: old therapies and new strategies. Lancet Infectious Disease 5 549557CrossRefGoogle ScholarPubMed
Avberse, J, Janezic, S, Patee, M, Rupnik, M, Zidaric, M, Logar, K, Vengust, M, Zemljic, M, Pirs, T & Ocepek, M 2009 Diversity of Clostridium difficile in pigs and other animals in Slovenia. Anaerobe 15 252255Google Scholar
Barth, H, Aktories, K, Popoff, MR & Stiles, BG 2004 Binary bacterial toxins: biochemistry, biology and applications of common Clostridium and Bacillus proteins. Microbiology and Molecular Biology Reviews 68 373402Google Scholar
Buts, JP 2008 Twenty-five years of research on Saccharomyces boulardii trophic effects: updates and perspectives. Digestive Disease Science 54 1518Google Scholar
Castagliuolo, I, LaMont, JT, Nikulasson, ST & Pothoulakis, C 1999 Saccharomyces boulardii protease inhibits Clostridium difficile toxin A effects in the rat ileum. Infection and Immunity 64 52255232Google Scholar
Chang, TW, Bartlett, LG, Gorbach, SL & Onderdonk, AB 1978 Clindamycin-induced enterocolitis in hamsters as a model of pseudomembranous colitis in patients. Infection and Immunity 20 526529Google Scholar
Cohen, SH, Gerding, DN, Johnson, S, Kelly, CP, Loo, VG, McDonald, LC, Pepin, J & Wilcox, MH 2010 Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA). Infection Control and Hospital Epidemiology 31 431455Google Scholar
Gomez Zavaglia, A, Kociubinski, G, Pérez, PF & De Antoni, GL 1998 Isolation and characterization of Bifidobacterium strains for probiotic formulation. Journal of Food Protection 61 865873Google Scholar
Gougoulias, C, Tuohy, KM & Gibson, GR 2007 Dietary-based gut flora modulation against Clostridium difficile onset. Food Science and Technology Bulletin: Functional Foods 4 3141Google Scholar
Gursoy, S, Guven, T, Arikan, K, Yurci, A, Torun, E, Baskol, EM, Ozbakir, O & Yucesoy, M 2007 Clostridium difficile infection frequency in patients with nosocomial infections or using antibiotics. Hepatogastroenterology 54 17201724Google Scholar
Hopman, NE, Keessen, EC, Harmanus, C, Sanders, IM, van Leengoed, LA, Kuijper, EJ & Lipman, LJ 2011 Acquisition of Clostridium difficile by piglets. Veterinary Microbiology 149 186192Google Scholar
Jank, T, Giesemann, T & Aktories, K 2007 Rho-glucosylating Clostridium difficile toxins A and B: new insights into structure and function. Glycobiology 17 15R22RGoogle Scholar
Kelly, CP, Pothoulakis, C & LaMont, JT 1994 Clostridium difficile colitis. New England Journal of Medicine 330 257262Google Scholar
Larson, HE & Borriello, SP 1990 Quantitative study of antibiotic-induced susceptibility to Clostridium difficile enterocecitis in hamsters. Antimicrobials Agents and Chemotherapy 34 13481353Google Scholar
Lewis, S, Burmeister, S & Brazier, J 2005 Effect of the probiotic oligofructose on relapse of Clostridium difficile-associated diarrhea: a randomized, controlled study. Clinical Gastroenterology and Hepatology 3 442448Google Scholar
Limaye, AP, Turgeon, DK, Cookson, BT & Fritsche, TR 2000 Pseudomembranous colitis caused by a toxin A(−) B(+) strain of Clostridium difficile. Journal of Clinical Microbiology 38 16961697Google Scholar
Lyras, D, O'Connor, JR, Howarth, PM, Sambol, SP, Carter, GP, Phumoonna, T, Poon, R, Adams, V, Vedantam, G, Johnson, S, Gerding, DM & Rood, JI 2009 Toxin B is essential for virulence of Clostridium difficile. Nature 458 11761179Google Scholar
Matsuki, S, OzakI, E, Shozu, M, Inoue, M, Shimizu, S, Yamaguchi, N, Karasawa, T, Yamagishi, T & Nakamura, S 2005 Colonization by Clostridium difficile of neonates in a hospital and infants and children in three day-care facilities of Kanazawa, Japan. International Microbiology 8 4348Google Scholar
McDonald, LC, Killgore, GE, Thompson, A, Owens, RC, Kazakova, VC, Sambol, SP, Johnson, S, & Gerding, DN 2005 An epidemic, toxin gene-variant strain of Clostridium difficile. New England Journal of Medicine 353 24332441Google Scholar
Musher, DM, Aslam, S, Logan, N, Nallacheru, S, Bhaila, I, Borchert, F & Hamill, RJ 2005 Relatively poor outcome after treatment of Clostridium difficile colitis with metronidazole. Clinical Infectious Diseases 40 15861590Google Scholar
Pepin, J, Alary, ME, Valiquette, L, Raiche, E, Ruel, J, Fulop, K, Godin, D & Bourassa, C 2005 Increasing risk of relapse after treatment of Clostridium difficile colitis in Quebec, Canada. Clinical Infectious Diseases 40 15911597Google Scholar
Pérez, PF, Minnaard, J, Disalvo, EA & De Antoni, GL 1998 Surface properties of bifidobacterial strains of human origin. Applied Environmental Microbiology 64 2126Google Scholar
Plummer, S, Weaver, MA, Harris, JC, Dee, P & Hunter, J 2004 Clostridium difficile pilot study: effects of probiotic supplementation on the incidence of C. difficile diarrhoea. International Microbiology 7 5962Google Scholar
Popoff, MR, Rubin, EJ, Gill, DM & Boquet, P 1988 Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain. Infection and Immunity 56 22992306Google Scholar
Sambol, SP, Merrigan, MM, Tang, JK, Johnson, S & Gerding, DN 2002 Colonization for the prevention of Clostridium difficile disease in hamsters. Journal of Infectious Diseases 186 17811789Google Scholar
Schroeder, M 2005 Clostridium difficile associated diarrhea. American Family Physician 71 921928Google Scholar
Schwan, C, Stecher, B, Tzivelekidis, T, van Ham, V, Rohde, M, Hardt, WD, Wehland, J & Aktories, K 2009 Clostridium difficile toxin CDT induces formation of microtubule-based protrusions and increases adherence of bacteria. PLoS Pathogens 5 e10000626. doi: 10.1371/journal.ppat.1000626CrossRefGoogle ScholarPubMed
Segarra-Newnham, M 2007 Probiotics for Clostridium difficile associated diarrhea: focus on Lactobacillus rhamnosus GG and Saccharomyces boulardii. Annals of Pharmacotherapy 41 12841287Google Scholar
Songer, JG & Anderson, MA 2006 Clostridium difficile: an important pathogen of food animals. Anaerobe 12 14CrossRefGoogle ScholarPubMed
Sunenshine, RH & McDonald, LC 2006 Clostridium difficile-associated disease: new challenges from an established pathogen. Cleveland Clinical Journal of Medicine 73 187197Google Scholar
Toothaker, RD & Elmer, GW 1984 Prevention of clindamycin-induced mortality in hamsters by Saccharomyces boulardii. Antimicrobial Agents and Chemotherapy 26 552556Google Scholar
Trejo, FM, Minnaard, J, Pérez, PF & De Antoni, GL 2006 Inhibition of Clostridium difficile growth and adhesion to enterocytes by Bifidobacterium supernatants. Anaerobe 12 186193Google Scholar
Trejo, FM, Pérez, PF & De Antoni, GL 2010 Co-culture with potentially probiotic microorganisms antagonises virulence factors of Clostridium difficile in vitro. Antonie van Leeuwenhoek 98 1929Google Scholar
Waters, EH, Orr, JP, Clark, EG & Schaufele, CM 1998 Typhlocolitis caused by Clostridium difficile in suckling piglets. Journal of Veterinary Diagnostic Investigation 10 104108Google Scholar
Wullt, M, Hagslatt, ML & Odenholt, I 2003 Lactobacillus plantarum 299v for the treatment of recurrent Clostridium difficile-associated diarrhoea: a double-blind, placebocontrolled trial. Scandinavian Journal of Infectious Diseases 35 365367Google Scholar
Xiao, JZ, Takahashi, S, Odamaki, T, Yaeshima, T & Iwatsuki, K 2010 Antibiotic susceptibility of bifidobacterial strains distributed in the Japanese market. Bioscience Biotechnology and Biochemistry 74 336342CrossRefGoogle ScholarPubMed