The DOI matches its Crossref record; 47 of the 47 references it cites were found in a registry or an index.
Suppression of Clostridium difficile in the Gastrointestinal Tracts of Germfree Mice Inoculated with a Murine Isolate from the Family Lachnospiraceae
Open accessAbstract
The indigenous microbial community of the gastrointestinal (GI) tract determines susceptibility to Clostridium difficile colonization and disease. Previous studies have demonstrated that antibiotic-treated mice challenged with C. difficile either developed rapidly lethal C. difficile infection or were stably colonized with mild disease. The GI microbial community of animals with mild disease was dominated by members of the bacterial family Lachnospiraceae, while the gut community in moribund animals had a predominance of Escherichia coli. We investigated the roles of murine Lachnospiraceae and E. coli strains in colonization resistance against C. difficile in germfree mice. Murine Lachnospiraceae and E. coli isolates were cultured from wild-type mice. The ability of each of these isolates to interfere with C. difficile colonization was tested by precolonizing germfree mice with these bacteria 4 days prior to experimental C. difficile challenge. Mice precolonized with a murine Lachnospiraceae isolate, but not those colonized with E. coli, had significantly decreased C. difficile colonization, lower intestinal cytotoxin levels and exhibited less severe clinical signs and colonic histopathology. Infection of germfree mice or mice precolonized with E. coli with C. difficile strain VPI 10463 was uniformly fatal by 48 h, but only 20% mortality was seen at 2 days in mice precolonized with the Lachnospiraceae isolate prior to challenge with VPI 10463. These findings confirm that a single component of the GI microbiota, a murine Lachnospiraceae isolate, could partially restore colonization resistance against C. difficile. Further study of the members within the Lachnospiraceae family could lead to a better understanding of mechanisms of colonization resistance against C. difficile and novel therapeutic approaches for the treatment and prevention of C. difficile infection.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Furthermore successful FMT restores members of Lachnospiraceae and other butyrate producing organisms supporting their potential role in outcompeting C. difficile.50”
From Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook (2015) · cites this paper as [50]
In the citing paper
“Additionally, changes in microbial community structure such as restoration of key Firmicutes and Bacteroidetes species with a decrease in Proteobacteria appear to be required in order to outcompete C. difficile.50”
From Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook (2015) · cites this paper as [50]
In the citing paper
“An important factor determining success of fecal transplant is restoration of microbial diversity following treatment50.”
From Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook (2015) · cites this paper as [50]
In the citing paper
“Bacterial strains [54, 118, 119] and metabolites [54] associated with protection from C. difficile have now been identified”
From Antibiotic-Induced Changes in the Intestinal Microbiota and Disease (2016) · cites this paper as [119]
Citations
Cites
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., et al. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.01541-09 · Cited by 19,549
Frank, D. N., St. Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., & Pace, N. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706625104 · Cited by 4,611
Colonic Health: Fermentation and Short Chain Fatty Acids
Wong, J. M. W., de Souza, R., Kendall, C. W. C., Emam, A., & Jenkins, D. J. A. (2006) · Journal of Clinical Gastroenterology · doi:10.1097/00004836-200603000-00015 · Cited by 2,739
Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach
Manichanh, C., Rigottier-Gois, L., Bonnaud, E., Gloux, K., Pelletier, E., Frangeul, L., Nalin, R., Jarrin, C., Chardon, P., Marteau, P., et al. (2006) · Gut · doi:10.1136/gut.2005.073817 · Cited by 2,277
Louis, P., & Flint, H. J. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01514.x · Cited by 2,179
Collins, M. D., Lawson, P. A., Willems, A., Córdoba, J. J., Fernández‐Garayzábal, J. F., GARCIA, P., Cai, J., Hippe, H., & Farrow, J. A. E. (1994) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-44-4-812 · Cited by 1,690
The microbiology of butyrate formation in the human colon
Pryde, S. E., Duncan, S. H., Hold, G. L., Stewart, C. S., & Flint, H. J. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11467.x · Cited by 1,320
Phylogenetic Relationships of Butyrate-Producing Bacteria from the Human Gut
Barcenilla, A., Pryde, S. E., Martin, J. C., Duncan, S. H., Stewart, C. S., Henderson, C., & Flint, H. J. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.4.1654-1661.2000 · Cited by 996
Colonization resistance of the digestive tract in conventional and antibiotic-treated mice
van der Waaij, D., Vries, J. M. B.-D., & der Wees, J. E. C. L.-V. (1971) · Journal of Hygiene · doi:10.1017/s0022172400021653 · Cited by 907
INTESTINAL FLORA IN NEW-BORN INFANTS
Hall, I. C. (1935) · American journal of diseases of children · doi:10.1001/archpedi.1935.01970020105010 · Cited by 766
Falk, P. G., Hooper, L. V., Midtvedt, T., & Gordon, J. I. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.4.1157-1170.1998 · Cited by 658
Frank, D. N., Robertson, C. E., Hamm, C. M., Kpadeh, Z. Z., Zhang, T., Chen, H., Zhu, W., Sartor, R. B., Boedeker, E. C., Harpaz, N., et al. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21339 · Cited by 612
A mouse model of clostridium difficile-associated disease
Chen, X., Katchar, K., Goldsmith, J. D., Nanthakumar, N., Cheknis, A., Gerding, D. N., & Kelly, C. P. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.09.002 · Cited by 510
Vollaard, E. J., & Clasener, H. A. (1994) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.38.3.409 · Cited by 478
Clindamycin-Associated Colitis Due to a Toxin-Producing Species of Clostridium in Hamsters
Bartlett, J. G., Onderdonk, A. B., Cisneros, R. L., & Kasper, D. L. (1977) · The Journal of Infectious Diseases · doi:10.1093/infdis/136.5.701 · Cited by 471
New Strategies for Cultivation and Detection of Previously Uncultured Microbes
Stevenson, B. S., Eichorst, S. A., Wertz, J. T., Schmidt, T. M., & Breznak, J. A. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.8.4748-4755.2004 · Cited by 443
Cultivable bacterial diversity from the human colon
Duncan, S. H., Louis, P., & Flint, H. J. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02129.x · Cited by 279
Reeves, A. E., Theriot, C. M., Bergin, I. L., Huffnagle, G. B., Schloss, P. D., & Young, V. B. (2011) · Gut Microbes · doi:10.4161/gmic.2.3.16333 · Cited by 277
Self-citationBritton, R. A., & Young, V. B. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.04.001 · Cited by 244
Self-citationNeutrophil recruitment in Clostridium difficile toxin A enteritis in the rabbit.
Kelly, C. P., Becker, S., Linevsky, J. K., Joshi, M. A., O’Keane, J. C., Dickey, B. F., LaMont, J. T., & Pothoulakis, C. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117080 · Cited by 200
Theriot, C. M., Koumpouras, C. C., Carlson, P. E., Bergin, I. L., Aronoff, D. M., & Young, V. B. (2011) · Gut Microbes · doi:10.4161/gmic.19142 · Cited by 190
Self-citationHopkins, M. J., & Macfarlane, G. T. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.4.1920-1927.2003 · Cited by 186
Colonization resistance of the digestive tract of mice during systemic antibiotic treatment
van der Waaij, D., Vries, J. M. B.-D., & der Wees, J. E. C. L.-V. (1972) · Epidemiology and Infection · doi:10.1017/s0022172400022464 · Cited by 169
May, T., Mackie, R. I., Fahey, G. C., Jr., Cremin, J. C., & Garleb, K. A. (1994) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365529409094863 · Cited by 160
Khanna, S., & Pardi, D. S. (2010) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/egh.10.48 · Cited by 159
The Microecology of Clostridium difficile
Wilson, K. H. (1993) · Clinical Infectious Diseases · doi:10.1093/clinids/16.supplement_4.s214 · Cited by 142
Role of volatile fatty acids in colonization resistance to Clostridium difficile
Rolfe, R. D. (1984) · Infection and Immunity · doi:10.1128/iai.45.1.185-191.1984 · Cited by 142
Rousseau, C., Levenez, F., Fouqueray, C., Dore, J. M., Collignon, A., & Lepage, P. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.01507-10 · Cited by 138
van der Waaij, D., Vries, J. M. B.-D., & der Wees, J. E. C. L.-V. (1972) · Journal of Hygiene · doi:10.1017/s0022172400022385 · Cited by 124
The role of antimicrobial agents in the aetiology of Clostridium difficile-associated disease
Spencer, R. C. (1998) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/41.suppl_3.21 · Cited by 121
Wilson, K. H., Silva, J., & Fekety, F. R. (1981) · Infection and Immunity · doi:10.1128/iai.34.2.626-628.1981 · Cited by 115
The Family Lachnospiraceae, Including the Genera Butyrivibrio, Lachnospira and Roseburia
Cotta, M. A., & Forster, R. J. (2006) · Springer eBooks · doi:10.1007/0-387-30744-3_35 · Cited by 112
Inhibition of Clostridium difficile strains by intestinal Lactobacillus species
Naaber, P., Smidt, I., Štšepetova, J., Brilene, T., Annuk, H., & Mikelsaar, M. (2004) · Journal of Medical Microbiology · doi:10.1099/jmm.0.45595-0 · Cited by 106
Clostridium clostridioforme: a mixture of three clinically important species
Finegold, S. M., Song, Y., Liu, C., Hecht, D. W., Summanen, P. H., Könönen, E., & Allen, S. D. (2005) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-005-1334-6 · Cited by 101
Wilson, K. H., Sheagren, J. N., & Freter, R. (1985) · The Journal of Infectious Diseases · doi:10.1093/infdis/151.2.355 · Cited by 100
Gnotobiotic Models for Study of the Microbial Ecology of Clostridium difficile and Escherichia coli
Wilson, K. H., Sheagren, J. N., Freter, R., Weatherbee, L., & Lyerly, D. M. (1986) · The Journal of Infectious Diseases · doi:10.1093/infdis/153.3.547 · Cited by 97
Corthier, G., Dubos, F., & Raibaud, P. (1985) · Applied and Environmental Microbiology · doi:10.1128/aem.49.1.250-252.1985 · Cited by 96
Clostridium difficile: progress and challenges
Bartlett, J. G. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05863.x · Cited by 87
Wilson, K. H., & Freter, R. R. (1986) · Infection and Immunity · doi:10.1128/iai.54.2.354-358.1986 · Cited by 77
Hedberg, M. E., Moore, E. R. B., Svensson‐Stadler, L., Hörstedt, P., Baranov, V. I., Hernell, O., Wai, S. N., Hammarström, S., & Hammarström, M. (2012) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.033613-0 · Cited by 69
Gorbach, S. L., Barza, M. J., Giuliano, M., & Jacobus, N. V. (1988) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/bf01962192 · Cited by 61
Clostridium difficile infection: The scope of the problem
Dubberke, E. R. (2012) · Journal of Hospital Medicine · doi:10.1002/jhm.1916 · Cited by 44
Role of volatile fatty acids in colonization resistance to Clostridium difficile in gnotobiotic mice
Su, W. J., Waechter, M., Bourlioux, P., Dolegeal, M., Fourniat, J., & Mahuzier, G. (1987) · Infection and Immunity · doi:10.1128/iai.55.7.1686-1691.1987 · Cited by 32
Clostridium difficile infection and inflammatory bowel disease: a marker for disease extent?
Powell, N., Jung, S.-W., & Krishnan, B. (2008) · PubMed · Cited by 28
Fekety, R., Silva, J., Browne, R., Rifkin, G. D., & Ebright, J. (1979) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/32.1.244 · Cited by 24
Intestinal bacteria antagonistic to Clostridium difficile in mice
Itoh, K., Lee, W. K., Kawamura, H., MITSUOKA, T., & Magaribuchi, T. (1987) · Laboratory Animals · doi:10.1258/002367787780740662 · Cited by 21
EXPLANATION FOR LIMITATION OF POPULATIONS OF ESCHERICHIA COLI IN BROTH CULTURES
Freter, R., & Ozawa, A. (1963) · Journal of Bacteriology · doi:10.1128/jb.86.5.904-910.1963 · Cited by 10
Cited by
Sorted by citations
Control of pathogens and pathobionts by the gut microbiota
Kamada, N., Chen, G. Y., Inohara, N., & Núñez, G. (2013) · Nature Immunology · doi:10.1038/ni.2608 · Cited by 1,625
Microbiota-mediated colonization resistance against intestinal pathogens
Buffie, C. G., & Pamer, E. G. (2013) · Nature reviews. Immunology · doi:10.1038/nri3535 · Cited by 1,564
Antibiotic-Induced Changes in the Intestinal Microbiota and Disease
Becattini, S., Taur, Y., & Pamer, E. G. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.04.003 · Cited by 901
Taur, Y., Jenq, R. R., Perales, M.-A., Littmann, E. R., Morjaria, S., Ling, L., No, D., Gobourne, A., Viale, A., Dahi, P. B., et al. (2014) · Blood · doi:10.1182/blood-2014-02-554725 · Cited by 885
Metadata
- Authors
- Reeves, A. E., Koenigsknecht, M. J., Bergin, I. L., & Young, V. B.
- Affiliations
- University of Michigan (US)
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2012-11
- Volume
- 80
- Issue
- 11
- Pages
- 3786-3794
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC3486043
- OpenAlex
- W2122459017
- Cited by
- 292
- References
- 47
- Citations by year
- 2026: 7 · 2025: 14 · 2024: 14 · 2023: 13 · 2022: 25 · 2021: 32 · 2020: 25 · 2019: 23 · 2018: 28 · 2017: 21 · 2016: 23 · 2015: 26 · 2014: 23 · 2013: 18
- FWCI
- 14.80
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Infection and Immunity (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (U19AI090871, AI090871)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK089503, R01DK070875, P30DK089503)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- Clostridium difficile, colonization resistance, Lachnospiraceae, gut microbiota, germ-free mice, Escherichia coli, Clostridium difficile infection, colonic histopathology, antibiotic-treated mice
- MeSH terms
- Animals, Escherichia coli, Germ-Free Life, Mice, Inbred C57BL, Phylogeny, RNA, Ribosomal, 16S, Colony Count, Microbial, Clostridioides difficile, Gram-Positive Endospore-Forming Rods, Gastrointestinal Tract, Mice, Metagenome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
