Role of the intestinal microbiota in resistance to colonization by Clostridium difficile

Gastroenterology

Volumn 146, Issue 6, 2014, Pages 1547-1553

  Britton, Robert A ^a   Young, Vincent B ^b  

^a Michigan State University ^*  (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Antibiotics; C difficile; Colonization Resistance; Microbial Ecology; Microbiome

Indexed keywords

ANTIBIOTIC AGENT; BILE SALT; CHENODEOXYCHOLIC ACID; CHOLIC ACID; CLINDAMYCIN; PROBIOTIC AGENT; SIALIC ACID DERIVATIVE;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL SPORE; CARBON SOURCE; CLOSTRIDIUM DIFFICILE INFECTION; COLITIS; COMMUNITY STRUCTURE; DRUG SAFETY; FECES MICROFLORA; HEALTH CARE COST; HUMAN; INTESTINE FLORA; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; NONHUMAN; PRIORITY JOURNAL; SPORE GERMINATION; VEGETATIVE GROWTH;

ANTIBIOTICS; C DIFFICILE; COLONIZATION RESISTANCE; MICROBIAL ECOLOGY; MICROBIOME;

ANIMALS; ANTI-BACTERIAL AGENTS; BILE ACIDS AND SALTS; BIOLOGICAL THERAPY; CLOSTRIDIUM DIFFICILE; DISEASE MODELS, ANIMAL; DYSBIOSIS; ENTEROCOLITIS, PSEUDOMEMBRANOUS; FECES; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; MICROBIOTA; PROBIOTICS;

EID: 84898771460     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.01.059     Document Type: Article

References (67)

1. J.G. Bartlett, A.B. Onderdonk, and R.L. Cisneros et al. Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters J Infect Dis 136 1977 701 705
2. I.C. Hall, and E. O'Toole Intestinal flora in new-born infants with the description of a new pathogenic anaerobe, Bacillus difficilis Am J Dis Child 49 1935 390 402
3. C.M. Thompson Jr., P.H. Gilligan, and M.C. Fisher et al. Clostridium difficile cytotoxin in a pediatric population Am J Dis Child 137 1983 271 274
4. C. Rousseau, I. Poilane, and L. De Pontual et al. Clostridium difficile carriage in healthy infants in the community: a potential reservoir for pathogenic strains Clin Infect Dis 55 2012 1209 1215
5. M.C. Rea, O. O'Sullivan, and F. Shanahan et al. Clostridium difficile carriage in elderly subjects and associated changes in the intestinal microbiota J Clin Microbiol 50 2012 867 875
6. D.E. Voth, and J.D. Ballard Clostridium difficile toxins: mechanism of action and role in disease Clin Microbiol Rev 18 2005 247 263
7. R.N. Pruitt, and D.B. Lacy Toward a structural understanding of Clostridium difficile toxins A and B Front Cell Infect Microbiol 2 2012 28
8. A. Shen Clostridium difficile toxins: mediators of inflammation J Innate Immun 4 2012 149 158
9. G. Hecht, C. Pothoulakis, and J.T. LaMont et al. Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers J Clin Invest 82 1988 1516 1524
10. I. Just, G. Fritz, and K. Aktories et al. Clostridium difficile toxin B acts on the GTP-binding protein Rho J Biol Chem 269 1994 10706 10712
11. C.P. Kelly, S. Becker, and J.K. Linevsky et al. Neutrophil recruitment in Clostridium difficile toxin A enteritis in the rabbit J Clin Invest 93 1994 1257 1265
12. E.E. Hamm, D.E. Voth, and J.D. Ballard Identification of Clostridium difficile toxin B cardiotoxicity using a zebrafish embryo model of intoxication Proc Natl Acad Sci U S A 103 2006 14176 14181
13. G. Vedantam, A. Clark, and M. Chu et al. Clostridium difficile infection: toxins and non-toxin virulence factors, and their contributions to disease establishment and host response Gut Microbes 3 2012 121 134
14. M. Rupnik, M. Grabnar, and B. Geric Binary toxin producing Clostridium difficile strains Anaerobe 9 2003 289 294
15. B.G. Stiles, D.J. Wigelsworth, and M.R. Popoff et al. Clostridial binary toxins: iota and C2 family portraits Front Cell Infect Microbiol 1 2011 11
16. L.C. McDonald, G.E. Killgore, and A. Thompson et al. An epidemic, toxin gene-variant strain of Clostridium difficile N Engl J Med 353 2005 2433 2441
17. J. Pepin, L. Valiquette, and M.E. Alary et al. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity CMAJ 171 2004 466 472
18. J. Freeman, M.P. Bauer, and S.D. Baines et al. The changing epidemiology of Clostridium difficile infections Clin Microbiol Rev 23 2010 529 549
19. E. Dubberke Clostridium difficile infection: the scope of the problem J Hosp Med 7 Suppl 3 2012 S1 S4
20. A. Goorhuis, D. Bakker, and J. Corver et al. Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078 Clin Infect Dis 47 2008 1162 1170
21. S.T. Walk, D. Micic, and R. Jain et al. Clostridium difficile ribotype does not predict severe infection Clin Infect Dis 55 2012 1661 1668
22. L.M. Proctor The Human Microbiome Project in 2011 and beyond Cell Host Microbe 10 2011 287 291
23. Human Microbiome Project C A framework for human microbiome research Nature 486 2012 215 221
24. M. Arumugam, J. Raes, and E. Pelletier et al. Enterotypes of the human gut microbiome Nature 473 2011 174 180
25. R. Freter The fatal enteric cholera infection in the guinea pig, achieved by inhibition of normal enteric flora J Infect Dis 97 1955 57 65
26. M. Bohnhoff, B.L. Drake, and C.P. Miller Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection Proc Soc Exp Biol Med 86 1954 132 137
27. E.A. Wadolkowski, D.C. Laux, and P.S. Cohen Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of growth in mucus Infect Immun 56 1988 1030 1035
28. E.A. Wadolkowski, J.A. Burris, and A.D. O'Brien Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157:H7 Infect Immun 58 1990 2438 2445
29. D.A. Antonopoulos, S.M. Huse, and H.G. Morrison et al. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation Infect Immun 77 2009 2367 2375
30. L. Dethlefsen, S. Huse, and M.L. Sogin et al. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing PLoS Biol 6 2008 e280
31. C.J. Robinson, and V.B. Young Antibiotic administration alters the community structure of the gastrointestinal micobiota Gut Microbes 1 2010 279 284
32. C.J. Robinson, B.J. Bohannan, and V.B. Young From structure to function: the ecology of host-associated microbial communities Microbiol Mol Biol Rev 74 2010 453 476
33. R.H. Lusk, R. Fekety, and J. Silva et al. Clindamycin-induced enterocolitis in hamsters J Infect Dis 137 1978 464 475
34. G.L. Peterfreund, L.E. Vandivier, and R. Sinha et al. Succession in the gut microbiome following antibiotic and antibody therapies for Clostridium difficile PLoS One 7 2012 e46966
35. X. Chen, K. Katchar, and J.D. Goldsmith et al. A mouse model of Clostridium difficile-associated disease Gastroenterology 135 2008 1984 1992
36. C.M. Theriot, C.C. Koumpouras, and P.E. Carlson et al. Cefoperazone-treated mice as an experimental platform to assess differential virulence of Clostridium difficile strains Gut Microbes 2 2011 326 334
37. A.E. Reeves, C.M. Theriot, and I.L. Bergin et al. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection Gut Microbes 2 2011 145 158
38. C.G. Buffie, I. Jarchum, and M. Equinda et al. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis Infect Immun 80 2012 62 73
39. A.E. Reeves, M.J. Koenigsknecht, and I.L. Bergin et al. Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae Infect Immun 80 2012 3786 3794
40. T.D. Lawley, S. Clare, and A.W. Walker et al. Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice PLoS Pathog 8 2012 e1002995
41. J.Y. Chang, D.A. Antonopoulos, and A. Kalra et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea J Infect Dis 197 2008 435 438
42. A. Petrof, and E. Khoruts From stool transplants to next-generation microbiota therapeutics Gastroenterology 146 2014 1573 1582
43. R.A. Britton, and V.B. Young Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance Trends Microbiol 20 2012 313 319
44. A. Howerton, N. Ramirez, and E. Abel-Santos Mapping interactions between germinants and Clostridium difficile spores J Bacteriol 193 2011 274 282
45. J.A. Sorg, and A.L. Sonenshein Bile salts and glycine as co-germinants for Clostridium difficile spores J Bacteriol 190 2008 2505 2512
46. J.A. Sorg, and A.L. Sonenshein Chenodeoxycholate is an inhibitor of Clostridium difficile spore germination J Bacteriol 191 2009 1115 1117
47. K.H. Wilson Efficiency of various bile salt preparations for stimulation of Clostridium difficile spore germination J Clin Microbiol 18 1983 1017 1019
48. L.C. Antunes, and B.B. Finlay A comparative analysis of the effect of antibiotic treatment and enteric infection on intestinal homeostasis Gut Microbes 2 2011 105 108
49. J.L. Giel, J.A. Sorg, and A.L. Sonenshein et al. Metabolism of bile salts in mice influences spore germination in Clostridium difficile PLoS One 5 2010 e8740
50. E. Krag, and S.F. Phillips Active and passive bile acid absorption in man. Perfusion studies of the ileum and jejunum J Clin Invest 53 1974 1686 1694
51. H.S. Mekhjian, S.F. Phillips, and A.F. Hofmann Colonic absorption of unconjugated bile acids: perfusion studies in man Dig Dis Sci 24 1979 545 550
52. E.R. Schiff, N.C. Small, and J.M. Dietschy Characterization of the kinetics of the passive and active transport mechanisms for bile acid absorption in the small intestine and colon of the rat J Clin Invest 51 1972 1351 1362
53. A. Howerton, M. Patra, and E. Abel-Santos A new strategy for the prevention of Clostridium difficile infection J Infect Dis 207 2013 1498 1504
54. M.B. Francis, C.A. Allen, and R. Shrestha et al. Bile acid recognition by the Clostridium difficile germinant receptor, CspC, is important for establishing infection PLoS Pathog 9 2013 e1003356
55. L. Bouillaut, W.T. Self, and A.L. Sonenshein Proline-dependent regulation of Clostridium difficile Stickland metabolism J Bacteriol 195 2013 844 854
56. S. Jackson, M. Calos, and A. Myers et al. Analysis of proline reduction in the nosocomial pathogen Clostridium difficile J Bacteriol 188 2006 8487 8495
57. T. Karasawa, S. Ikoma, and K. Yamakawa et al. A defined growth medium for Clostridium difficile Microbiology 141 1995 371 375
58. S. Nakamura, S. Nakashio, and K. Yamakawa et al. Carbohydrate fermentation by Clostridium difficile Microbiol Immunol 26 1982 107 111
59. K.H. Wilson, and F. Perini Role of competition for nutrients in suppression of Clostridium difficile by the colonic microflora Infect Immun 56 1988 2610 2614
60. K.M. Ng, J.A. Ferreyra, and S.K. Higginbottom et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens Nature 502 2013 96 99
61. R. Freter, H. Brickner, and M. Botney et al. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora Infect Immun 39 1983 676 685
62. K.H. Wilson The microecology of Clostridium difficile Clin Infect Dis 16 Suppl 4 1993 S214 S218
63. M. Merrigan, S. Sambol, and S. Johnson et al. Susceptibility of hamsters to human pathogenic Clostridium difficile strain B1 following clindamycin, ampicillin or ceftriaxone administration Anaerobe 9 2003 91 95
64. S.P. Sambol, M.M. Merrigan, and J.K. Tang et al. Colonization for the prevention of Clostridium difficile disease in hamsters J Infect Dis 186 2002 1781 1789
65. C. Vincent, D.A. Stephens, and V.G. Loo et al. Reductions in intestinal Clostridiales precede the development of nosocomial Clostridium difficile infection Microbiome 1 2013 18
66. M. Tvede, and J. Rask-Madsen Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients Lancet 1 1989 1156 1160
67. E.O. Petrof, G.B. Gloor, and S.J. Vanner et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: 'RePOOPulating' the gut Microbiome 1 2013 3