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.
Integrity signals
Registry
Cites
Statistics
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?
Successful FMT restores members of Lachnospiraceae and other butyrate-producing organisms, supporting their potential role in outcompeting C. difficile.
“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]
Changes in microbial community structure, including restoration of key Firmicutes and Bacteroidetes species and a decrease in Proteobacteria, appear required to outcompete C. difficile.
“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]
Restoration of microbial diversity is an important factor determining success of fecal transplant.
“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]
Bacterial strains and metabolites associated with protection from C. difficile have been identified.
“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]
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 20,966 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Louis, P., & Flint, H. J. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01514.x · Cited by 2,179 · see citing works
Collins, M. D., Lawson, P. A., Willems, A. L., 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 1,670 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 643 · see citing works
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 594 · see citing works
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 · see citing works
Vollaard, E. J., & Clasener, H. A. (1994) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.38.3.409 · Cited by 478 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 270 · see citing works
Self-citationBritton, R. A., & Young, V. B. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.04.001 · Cited by 236 · see citing works
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 · see citing works
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 · see citing works
Self-citationHopkins, M. J., & Macfarlane, G. T. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.4.1920-1927.2003 · Cited by 183 · see citing works
Colonization resistance of the digestive tract of mice during systemic antibiotic treatment
van der Waaij, D., Berghuis, J. M., & Lekkerkerk, J. E. C. (1972) · Epidemiology and Infection · doi:10.1017/s0022172400022464 · Cited by 172 · see citing works
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 · see citing works
Khanna, S., & Pardi, D. S. (2010) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/egh.10.48 · Cited by 159 · see citing works
The Microecology of Clostridium difficile
Wilson, K. H. (1993) · Clinical Infectious Diseases · doi:10.1093/clinids/16.supplement_4.s214 · Cited by 142 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Wilson, K. H., Silva, J., & Fekety, F. R. (1981) · Infection and Immunity · doi:10.1128/iai.34.2.626-628.1981 · Cited by 115 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Wilson, K. H., Sheagren, J. N., & Freter, R. (1985) · The Journal of Infectious Diseases · doi:10.1093/infdis/151.2.355 · Cited by 100 · see citing works
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 · see citing works
Corthier, G., Dubos, F., & Raibaud, P. (1985) · Applied and Environmental Microbiology · doi:10.1128/aem.49.1.250-252.1985 · Cited by 96 · see citing works
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 · see citing works
Wilson, K. H., & Freter, R. R. (1986) · Infection and Immunity · doi:10.1128/iai.54.2.354-358.1986 · Cited by 77 · see citing works
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 · see citing works
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 · see citing works
Clostridium difficile infection: The scope of the problem
Dubberke, E. R. (2012) · Journal of Hospital Medicine · doi:10.1002/jhm.1916 · Cited by 44 · see citing works
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 · see citing works
Clostridium difficile infection and inflammatory bowel disease: a marker for disease extent?
Powell, N., Jung, S.-W., & Krishnan, B. (2008) · PubMed · Cited by 28 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Flagged first, then by citations
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
The intestinal microbiota: Antibiotics, colonization resistance, and enteric pathogens
Kim, S., Covington, A., & Pamer, E. G. (2017) · Immunological Reviews · doi:10.1111/imr.12563 · Cited by 741 · see citing works
Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook
Kelly, C. R., Kahn, S., Kashyap, P., Laine, L., Rubin, D., Atreja, A., Moore, T., & Wu, G. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.05.008 · Cited by 572 · see citing works
Multi-omics analyses of radiation survivors identify radioprotective microbes and metabolites
Guo, H., Chou, W.-C., Lai, Y., Liang, K., Tam, J. W., Brickey, W. J., Chen, L., Montgomery, N. D., Li, X., Bohannon, L. M., et al. (2020) · Science · doi:10.1126/science.aay9097 · Cited by 561 · see citing works
Clostridium difficile colitis: pathogenesis and host defence
Abt, M. C., McKenney, P. T., & Pamer, E. G. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.108 · Cited by 552 · see citing works
Antharam, V. C., Li, E. C., Ishmael, A., Sharma, A., Mai, V., Rand, K. H., & Wang, G. P. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.00845-13 · Cited by 485 · see citing works
Dysbiosis of gut microbiota and microbial metabolites in Parkinson's disease
Sun, M.-F., & Shen, Y.-Q. (2018) · Ageing Research Reviews · doi:10.1016/j.arr.2018.04.004 · Cited by 445 · see citing works
Role of the Intestinal Microbiota in Resistance to Colonization by Clostridium difficile
Britton, R. A., & Young, V. B. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.01.059 · Cited by 446 · see citing works
Self-citationResurrecting the intestinal microbiota to combat antibiotic-resistant pathogens
Pamer, E. G. (2016) · Science · doi:10.1126/science.aad9382 · Cited by 423 · see citing works
Precision Nutrition and the Microbiome, Part I: Current State of the Science
Mills, S., Stanton, C., Lane, J. A., Smith, G., & Ross, R. P. (2019) · Nutrients · doi:10.3390/nu11040923 · Cited by 406 · see citing works
Manipulation of the Quorum Sensing Signal AI-2 Affects the Antibiotic-Treated Gut Microbiota
Thompson, J. A., Oliveira, R. A., Djuković, A., Úbeda, C., & Xavier, K. B. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.049 · Cited by 390 · see citing works
Taur, Y., Coyte, K. Z., Schlüter, J., Robilotti, E. V., Figueroa, C. J., Gjonbalaj, M., Littmann, E. R., Ling, L., Miller, L., Gyaltshen, Y., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aap9489 · Cited by 370 · see citing works
Avilés‐Jiménez, F., Vázquez‐Jiménez, F. E., Guzman, R. M., Mantilla, A., & Torres, J. (2014) · Scientific Reports · doi:10.1038/srep04202 · Cited by 340 · see citing works
Recovery of the Gut Microbiome following Fecal Microbiota Transplantation
Seekatz, A. M., Aas, J., Gessert, C. E., Rubin, T. A., Saman, D. M., Bakken, J., & Young, V. B. (2014) · mBio · doi:10.1128/mbio.00893-14 · Cited by 331 · see citing works
Self-citationUnderstanding Clostridium difficile Colonization
Crobach, M. J. T., Vernon, J. J., Loo, V. G., Kong, L. Y., Péchiné, S., Wilcox, M. H., & Kuijper, E. J. (2018) · Clinical Microbiology Reviews · doi:10.1128/cmr.00021-17 · Cited by 329 · see citing works
Pereira, F. C., Wasmund, K., Spreitzer, I., Jehmlich, N., Herbold, C. W., Lee, K. S., Szirányi, B., Vesely, C., Decker, T., Stocker, R., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18928-1 · Cited by 311 · see citing works
Chen, L., Wilson, J. E., Koenigsknecht, M. J., Chou, W.-C., Montgomery, S. A., Truax, A. D., Brickey, W. J., Packey, C. D., Maharshak, N., Matsushima, G. K., et al. (2017) · Nature Immunology · doi:10.1038/ni.3690 · Cited by 310 · see citing works
Self-citationCooperating Commensals Restore Colonization Resistance to Vancomycin-Resistant Enterococcus faecium
Caballero, S., Kim, S., Carter, R. A., Leiner, I. M., Sušac, B., Miller, L., Kim, G. J., Ling, L., & Pamer, E. G. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.04.002 · Cited by 308 · see citing works
Interactions Between the Gastrointestinal Microbiome and Clostridium difficile
Theriot, C. M., & Young, V. B. (2015) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091014-104115 · Cited by 301 · see citing works
Self-citationResveratrol-induced gut microbiota reduces obesity in high-fat diet-fed mice
Wang, P., Li, D., Ke, W., Liang, D., Hu, X., & Chen, F. (2020) · International Journal of Obesity · doi:10.1038/s41366-019-0332-1 · Cited by 301 · see citing works
Mechanism of the Gut Microbiota Colonization Resistance and Enteric Pathogen Infection
Khan, I., Bai, Y., Zha, L., Ullah, N., Ullah, H., Shah, S. R. H., Sun, H., & Zhang, C. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.716299 · Cited by 291 · see citing works
Schubert, A. M., Sinani, H., & Schloss, P. D. (2015) · mBio · doi:10.1128/mbio.00974-15 · Cited by 269 · see citing works
Zhang, C., Derrien, M., Levenez, F., Brazeilles, R., Ballal, S. A., Kim, J., Degivry, M.-C., Quéré, G., Garault, P., van Hylckama Vlieg, J. E. T., et al. (2016) · The ISME Journal · doi:10.1038/ismej.2016.13 · Cited by 264 · see citing works
Clostridium difficile and the microbiota
Seekatz, A. M., & Young, V. B. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72336 · Cited by 255 · see citing works
Self-citationHolm, J. B., Sorobetea, D., Kiilerich, P., Ramayo‐Caldas, Y., Estellé, J., Ma, T., Madsen, L., Kristiansen, K., & Svensson, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125495 · Cited by 248 · see citing works
Microbiome Dependent Regulation of Tregs and Th17 Cells in Mucosa
Pandiyan, P., Bhaskaran, N., Zou, M., Schneider, E., Jayaraman, S., & Huehn, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00426 · Cited by 231 · see citing works
Costa, M., Silva, G., Ramos, R. V., Staempfli, H. R., Arroyo, L. G., Kim, P., & Weese, J. S. (2015) · The Veterinary Journal · doi:10.1016/j.tvjl.2015.03.018 · Cited by 228 · see citing works
Kim, M., Hwang, S., Park, E., & Bae, J. (2013) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12079 · Cited by 220 · see citing works
Commensal bacteria mediated defenses against pathogens
Abt, M. C., & Pamer, E. G. (2014) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.03.003 · Cited by 212 · see citing works
Characterization of the 17 strains of regulatory T cell-inducing human-derived Clostridia
Narushima, S., Sugiura, Y., Oshima, K., Atarashi, K., Hattori, M., Suematsu, M., & Honda, K. (2014) · Gut Microbes · doi:10.4161/gmic.28572 · Cited by 210 · see citing works
Enlightening the taxonomy darkness of human gut microbiomes with a cultured biobank
Liu, C., Du, M., Abuduaini, R., Yu, H., Li, D., Wang, Y., Zhou, N., Jiang, M.-Z., Niu, P.-X., Han, S.-S., et al. (2021) · Microbiome · doi:10.1186/s40168-021-01064-3 · Cited by 205 · see citing works
Metabolite profiling of human‐originated Lachnospiraceae at the strain level
Abdugheni, R., Wang, W.-Z., Wang, Y., Du, M., Liu, F.-L., Zhou, N., Jiang, C., Wang, C., Wu, L., Ma, J., et al. (2022) · iMeta · doi:10.1002/imt2.58 · Cited by 193 · see citing works
Fecal Transplants: What Is Being Transferred?
Bojanova, D. P., & Bordenstein, S. R. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002503 · Cited by 190 · see citing works
Liu, Z., Chen, Z., Guo, H., He, D., Zhao, H., Wang, Z., Zhang, W., Liao, L., Zhang, C., & Ni, L. (2016) · Food & Function · doi:10.1039/c6fo01439a · Cited by 185 · see citing works
Zhou, R., He, D., Xie, J., Zhou, Q., Zeng, H., Li, H., & Huang, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.665901 · Cited by 185 · see citing works
Changes in the faecal microbiota of mares precede the development of post partum colic
Weese, J. S., Holcombe, S. J., Embertson, R. M., Kurtz, K. A., Roessner, H. A., Jalali, M., & Wismer, S. E. (2014) · Equine Veterinary Journal · doi:10.1111/evj.12361 · Cited by 184 · see citing works
Jiang, Z., Ajami, N. J., Petrosino, J. F., Jun, G., Hanis, C. L., Shah, M. S., Hochman, L. G., Ankoma‐Sey, V., DuPont, A. W., Wong, M. C., et al. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13969 · Cited by 182 · see citing works
From Hype to Hope: The Gut Microbiota in Enteric Infectious Disease
McKenney, P. T., & Pamer, E. G. (2015) · Cell · doi:10.1016/j.cell.2015.11.032 · Cited by 182 · see citing works
Clostridium difficile – From Colonization to Infection
Schäffler, H., & Breitrück, A. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00646 · Cited by 174 · see citing works
Li, M., Monaco, M. H., Wang, M., Comstock, S. S., Kuhlenschmidt, T. B., Fahey, G. C., Jr., Miller, M. J., Kuhlenschmidt, M. S., & Donovan, S. M. (2014) · The ISME Journal · doi:10.1038/ismej.2014.10 · Cited by 173 · see citing works
Murine colitis reveals a disease-associated bacteriophage community
Duerkop, B. A., Kleiner, M., Páez-Espino, D., Zhu, W., Bushnell, B., Hassell, B., Winter, S., Kyrpides, N. C., & Hooper, L. V. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0210-y · Cited by 165 · see citing works
Dynamics and Establishment of Clostridium difficile Infection in the Murine Gastrointestinal Tract
Koenigsknecht, M. J., Theriot, C. M., Bergin, I. L., Schumacher, C. A., Schloss, P. D., & Young, V. B. (2014) · Infection and Immunity · doi:10.1128/iai.02768-14 · Cited by 172 · see citing works
Self-citationSong, Y., Garg, S., Girotra, M., Maddox, C., von Rosenvinge, E. C., Dutta, A., Dutta, S., & Fricke, W. F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081330 · Cited by 169 · see citing works
The Effect of Trans Fatty Acids on Human Health: Regulation and Consumption Patterns
Pipoyan, D., Stepanyan, S., Stepanyan, S., Beglaryan, M., Costantini, L., Molinari, R., & Merendino, N. (2021) · Foods · doi:10.3390/foods10102452 · Cited by 161 · see citing works
Fiebiger, U., Bereswill, S., & Heimesaat, M. M. (2016) · European Journal of Microbiology and Immunology · doi:10.1556/1886.2016.00036 · Cited by 160 · see citing works
Umu, Ö. C. O., Frank, J. A., Fangel, J. U., Oostindjer, M., da Silva, C. S., Bolhuis, J. E., Bosch, G., Willats, W. G. T., Pope, P. B., & Diep, D. B. (2015) · Microbiome · doi:10.1186/s40168-015-0078-5 · Cited by 154 · see citing works
Winston, J. A., & Theriot, C. M. (2016) · Anaerobe · doi:10.1016/j.anaerobe.2016.05.003 · Cited by 150 · see citing works
Socioeconomic Status and the Gut Microbiome: A TwinsUK Cohort Study
Bowyer, R. C. E., Jackson, M. A., Le Roy, C. I., Ni Lochlainn, M., Spector, T. D., Dowd, J. B., & Steves, C. J. (2019) · Microorganisms · doi:10.3390/microorganisms7010017 · Cited by 150 · see citing works
Menon, R., Watson, S. E., Thomas, L. N., Allred, C. D., Dabney, A. R., Azcárate-Peril, M. A., & Sturino, J. M. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01182-13 · Cited by 146 · see citing works
Phạm, V. H., Kan, L., Huang, J., Geng, Y., Zhen, W., Guo, Y., Abbas, W., & Wang, Z. (2020) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-019-0421-y · Cited by 151 · see citing works
The intestinal microbiota and susceptibility to infection in immunocompromised patients
Taur, Y., & Pamer, E. G. (2013) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0b013e3283630dd3 · Cited by 137 · see citing works
Passmore, I. J., Letertre, M. P. M., Preston, M. D., Bianconi, I., Harrison, M. A., Nasher, F., Kaur, H., Hong, H. A., Baines, S. D., Cutting, S. M., et al. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007191 · Cited by 138 · see citing works
Modulation of post-antibiotic bacterial community reassembly and host response by Candida albicans
Erb Downward, J. R., Falkowski, N. R., Mason, K. L., Muraglia, R., & Huffnagle, G. B. (2013) · Scientific Reports · doi:10.1038/srep02191 · Cited by 136 · see citing works
Inference of Network Dynamics and Metabolic Interactions in the Gut Microbiome
Steinway, S. N., Biggs, M. B., Loughran, T. P., Papin, J. A., & Albert, R. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004338 · Cited by 127 · see citing works
Lachnospiraceae are emerging industrial biocatalysts and biotherapeutics
Zaplana, T., Miele, S., & Tolonen, A. C. (2024) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1324396 · Cited by 127 · see citing works
Commensal Gram-positive bacteria initiates colitis by inducing monocyte/macrophage mobilization
Nakanishi, Y., Sato, T., & Ohteki, T. (2014) · Mucosal Immunology · doi:10.1038/mi.2014.53 · Cited by 121 · see citing works
In vivo commensal control of Clostridioides difficile virulence
Girinathan, B. P., DiBenedetto, N., Worley, J. N., Peltier, J., Arrieta-Ortiz, M. L., Immanuel, S. R. C., Lavin, R., Delaney, M. L., Cummins, C. K., Hoffman, M., et al. (2021) · Cell Host & Microbe · doi:10.1016/j.chom.2021.09.007 · Cited by 114 · see citing works
Emerging insights on intestinal dysbiosis during bacterial infections
Pham, T. A. N., & Lawley, T. D. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.12.002 · Cited by 115 · see citing works
Fecal microbiota transplantation: effectiveness, complexities, and lingering concerns
Pamer, E. G. (2014) · Mucosal Immunology · doi:10.1038/mi.2013.117 · Cited by 109 · see citing works
Sewage reflects the distribution of human faecal L achnospiraceae
McLellan, S. L., Newton, R. J., VandeWalle, J. L., Shanks, O. C., Huse, S. M., Eren, A. M., & Sogin, M. L. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12092 · Cited by 109 · see citing works
Fletcher, J. R., Erwin, S., Lanzas, C., & Theriot, C. M. (2018) · mSphere · doi:10.1128/msphere.00089-18 · Cited by 104 · see citing works
Learning from bacterial competition in the host to develop antimicrobials
Raffatellu, M. (2018) · Nature Medicine · doi:10.1038/s41591-018-0145-0 · Cited by 110 · see citing works
Development of the faecal microbiota in foals
Costa, M., Stämpfli, H. R., Allen‐Vercoe, E., & Weese, J. S. (2015) · Equine Veterinary Journal · doi:10.1111/evj.12532 · Cited by 107 · see citing works
Pérez‐Cobas, A. E., Artacho, A., Ott, S. J., Moyá, A., Gosalbes, M. J., & Latorre, A. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00335 · Cited by 105 · see citing works
Rapid transcriptional and metabolic adaptation of intestinal microbes to host immune activation
Becattini, S., Sorbara, M. T., Kim, S. G., Littmann, E. R., Dong, Q., Walsh, G., Wright, R. J., Amoretti, L. A., Fontana, E., Hohl, T. M., et al. (2021) · Cell Host & Microbe · doi:10.1016/j.chom.2021.01.003 · Cited by 103 · see citing works
Peripheral education of the immune system by the colonic microbiota
Kuhn, K. A., & Stappenbeck, T. S. (2013) · Seminars in Immunology · doi:10.1016/j.smim.2013.10.002 · Cited by 104 · see citing works
Commensal Koch's postulates: establishing causation in human microbiota research
Neville, B. A., Forster, S. C., & Lawley, T. D. (2017) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.10.001 · Cited by 102 · see citing works
Marques, T. M., Wall, R., O’Sullivan, Ó., Fitzgerald, G. F., Shanahan, F., Quigley, E. M. M., Cotter, P. D., Cryan, J. F., Dinan, T. G., Ross, R. P., et al. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114514004206 · Cited by 101 · see citing works
Baktash, A., Terveer, E. M., Zwittink, R. D., Hornung, B., Corver, J., Kuijper, E. J., & Smits, W. K. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01242 · Cited by 102 · see citing works
Stecher, B., Berry, D., & Loy, A. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12024 · Cited by 101 · see citing works
Altered Egos: Antibiotic Effects on Food Animal Microbiomes
Allen, H. K., & Stanton, T. B. (2014) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091213-113052 · Cited by 99 · see citing works
Jenior, M. L., Leslie, J. L., Young, V. B., & Schloss, P. D. (2018) · mSphere · doi:10.1128/msphere.00261-18 · Cited by 96 · see citing works
Self-citationMechanisms of Microbe–Host Interaction in Crohn’s Disease: Dysbiosis vs. Pathobiont Selection
Buttó, L. F., Schaubeck, M., & Haller, D. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00555 · Cited by 92 · see citing works
Jump, R., Polinkovsky, A., Hurless, K. N., Sitzlar, B. M., Eckart, K. E., Tomas, M. E., Deshpande, A., Nerandzic, M. M., & Donskey, C. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101267 · Cited by 91 · see citing works
Microbiome mediation of infections in the cancer setting
Taur, Y., & Pamer, E. G. (2016) · Genome Medicine · doi:10.1186/s13073-016-0306-z · Cited by 89 · see citing works
Mefferd, C. C., Bhute, S. S., Phan, J. R., Villarama, J. V., Do, D. M., Alarcia, S., Abel‐Santos, E., & Hedlund, B. P. (2020) · mSystems · doi:10.1128/msystems.00765-19 · Cited by 88 · see citing works
Markey, L., Shaban, L., Green, E. R., Lemon, K. P., Mecsas, J. C., & Kumamoto, C. A. (2018) · Gut Microbes · doi:10.1080/19490976.2018.1465158 · Cited by 87 · see citing works
Enlisting commensal microbes to resist antibiotic-resistant pathogens
Keith, J. W., & Pamer, E. G. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20180399 · Cited by 87 · see citing works
Lee, Y. J., Argüello, E., Jenq, R. R., Littmann, E. R., Kim, G. J., Miller, L., Ling, L., Figueroa, C. J., Robilotti, E. V., Perales, M., et al. (2017) · The Journal of Infectious Diseases · doi:10.1093/infdis/jix011 · Cited by 83 · see citing works
Colonization Resistance of the Gut Microbiota against Clostridium difficile
Pérez‐Cobas, A. E., Moyá, A., Gosalbes, M. J., & Latorre, A. (2015) · Antibiotics · doi:10.3390/antibiotics4030337 · Cited by 82 · see citing works
Harrison, C. A., Laubitz, D., Ohland, C., Midura‐Kiela, M. T., Patil, K., Besselsen, D. G., Jamwal, D. R., Jobin, C., Ghishan, F. K., & Kiela, P. R. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0035-2 · Cited by 81 · see citing works
Small animal models for the study ofClostridium difficiledisease pathogenesis
Hutton, M. L., Mackin, K. E., Chakravorty, A., & Lyras, D. (2013) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12367 · Cited by 81 · see citing works
Preventive Effects and Mechanisms of Garlic on Dyslipidemia and Gut Microbiome Dysbiosis
Chen, K., Xie, K., Liu, Z., Nakasone, Y., Sakao, K., Hossain, M. A., & Hou, D.-X. (2019) · Nutrients · doi:10.3390/nu11061225 · Cited by 79 · see citing works
Theriot, C. M., & Young, V. B. (2013) · Gut Microbes · doi:10.4161/gmic.27131 · Cited by 80 · see citing works
Self-citationMicrobiologic factors affecting Clostridium difficile recurrence
Chilton, C. H., Pickering, D. S., & Freeman, J. (2017) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2017.11.017 · Cited by 80 · see citing works
Jenkins, T. P., Formenti, F., Castro, C., Piubelli, C., Perandin, F., Buonfrate, D., Otranto, D., Griffin, J. L., Krause, L., Bisoffi, Z., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-33937-3 · Cited by 78 · see citing works
Liu, W., Zhang, Y., Qiu, B., Fan, S., Ding, H., & Liu, Z. (2018) · Scientific Reports · doi:10.1038/s41598-018-33092-9 · Cited by 77 · see citing works
Jiang, L., Ye, Y., Han, Y., Wang, Q., Lu, H., Li, J., Qian, W., Zeng, X. Y., Zhang, Z., Zhao, Y., et al. (2024) · Cell Discovery · doi:10.1038/s41421-024-00665-0 · Cited by 86 · see citing works
Gu, S., Chen, Y., Zhang, X., Lu, H., Lv, T., Shen, P., Lv, L., Zheng, B., Jiang, X., & Li, L. (2015) · Microbes and Infection · doi:10.1016/j.micinf.2015.09.008 · Cited by 77 · see citing works
Morjaria, S. M., Schlüter, J., Taylor, B. P., Littmann, E. R., Carter, R. A., Fontana, E., Peled, J. U., van den Brink, M. R. M., Xavier, J. B., & Taur, Y. (2019) · Infection and Immunity · doi:10.1128/iai.00206-19 · Cited by 76 · see citing works
IL-17–producing γδ T cells protect against Clostridium difficile infection
Chen, Y.-S., Chen, I.-B. D., Pham, G. H., Shao, T., Bangar, H., Way, S. S., & Haslam, D. B. (2020) · Journal of Clinical Investigation · doi:10.1172/jci127242 · Cited by 76 · see citing works
Zhu, G., Jiang, Y., Yao, Y., Wu, N., Luo, J., Hu, M., Tu, Y., & Xu, M. (2019) · Food & Function · doi:10.1039/c8fo02312c · Cited by 74 · see citing works
Qing, Y., Xie, H., Su, C. H., Wang, Y., Yu, Q., Pang, Q., & Cui, F. (2018) · Digestive Diseases and Sciences · doi:10.1007/s10620-018-5428-2 · Cited by 74 · see citing works
Insights into the Role of Human Gut Microbiota in Clostridioides difficile Infection
Kachrimanidou, M., & Tsintarakis, E. (2020) · Microorganisms · doi:10.3390/microorganisms8020200 · Cited by 71 · see citing works
Muricholic Acids Inhibit Clostridium difficile Spore Germination and Growth
Francis, M. B., Allen, C. A., & Sorg, J. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073653 · Cited by 68 · see citing works
Gnotobiotic Rodents: An In Vivo Model for the Study of Microbe–Microbe Interactions
Martín, R., Bermúdez‐Humarán, L. G., & Langella, P. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00409 · Cited by 67 · see citing works
- 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
