The vexed relationship between Clostridium difficile and inflammatory bowel disease: an assessment of carriage in an outpatient setting among patients in remission.
Abstract
OBJECTIVES: Comorbidity with Clostridium difficile may cause diagnostic delay in newly presenting inflammatory bowel disease (IBD) patients, trigger relapse in established disease, confound therapies, and serve as an indicator of an underlying defect in innate immunity. Retrospective analyses have suggested community acquisition; to address this we conducted a prospective analysis of C. difficile carriage in IBD patients using molecular methods specifically in an outpatient setting. METHODS: Recruited participants had long-standing diagnoses of ulcerative colitis (n = 64) and Crohn's disease (n = 58), were in clinical remission, and had no recent exposure to antibiotics, corticosteroids, immunomodulatory drugs or recent hospitalization. Isolates were cultured from stools and confirmed by 16S sequencing. The antibiotic susceptibilities of the isolates were tested followed by further strain characterization by toxinotyping, ribotyping, and pulsed-field gel electrophoresis (PFGE). RESULTS: The frequency of toxigenic C. difficile was higher in IBD patients than in healthy volunteers at 8.2 and 1.0%, respectively (P = 0.02 Fisher's exact test). All strains belonged to toxinotype 0 with rare subtypes of this group noted in five isolates and represented by an altered repressor genotype. Patients harbored a diverse range of toxigenic ribotype groups, including those previously associated with C. difficile-associated disease (CDAD) (R015, R005, and R020) and the rarer types R062, R050, and R003. Interestingly, common nosocomial groups were not identified. The considerable nonclonal distribution of distinct strains was further demonstrated by PFGE genomic fingerprinting. None of the study subjects experienced a clinical episode of CDAD during a 6-month period of follow-up. CONCLUSIONS: Detection of C. difficile is increased in IBD outpatients in remission, and strain diversity is consistent with community acquisition from a multitude of sources.
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?
IBD patients have a higher asymptomatic C. difficile carriage status: as high as 8% compared to a rate of 1% in healthy subjects.
“IBD patients have a higher asymptomatic Cd carriage status: as high as 8% compared to a rate of 1% in healthy subjects 40.”
From Antibiotic treatment of acute gastroenteritis in children (2018) · cites this paper as [40]
Cites
Nosocomial Acquisition ofClostridium difficileInfection
McFarland, L. V., Mulligan, M. E., Kwok, R. Y. Y., & Stamm, W. E. (1989) · New England Journal of Medicine · doi:10.1056/nejm198901263200402 · Cited by 1,292 · see citing works
Asymptomatic Carriage ofClostridium difficileand Serum Levels of IgG Antibody against Toxin A
Kyne, L., Warny, M., Qamar, A., & Kelly, C. P. (2000) · New England Journal of Medicine · doi:10.1056/nejm200002103420604 · Cited by 932 · see citing works
Emergence of Clostridium difficile-associated disease in North America and Europe
Kuijper, E. J., Coignard, B., & Tüll, P. (2006) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2006.01580.x · Cited by 855 · see citing works
Impact of Clostridium difficile on Inflammatory Bowel Disease
Issa, M., Vijayapal, A., Graham, M. B., Beaulieu, D. B., Otterson, M. F., Lundeen, S. J., Skaros, S., Weber, L. R., KOMOROWSKI, R. A., Knox, J. F., et al. (2007) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2006.12.028 · Cited by 570 · see citing works
Stubbs, S. L. J., Brazier, J. S., O'Neill, G. L., & Duerden, B. I. (1999) · Journal of Clinical Microbiology · doi:10.1128/jcm.37.2.461-463.1999 · Cited by 547 · see citing works
Incidence of Clostridium difficile Infection in Inflammatory Bowel Disease
Rodemann, J. F., Dubberke, E. R., Reske, K. A., Seo, D. H., & Stone, C. D. (2007) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2006.12.027 · Cited by 520 · see citing works
Wiström, J. (2001) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/47.1.43 · Cited by 455 · see citing works
Stubbs, S. L. J., Rupnik, M., Gibert, M., Brazier, J., Duerden, B. I., & Popoff, M. R. (2000) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2000.tb09122.x · Cited by 438 · see citing works
Nguyen, G. C., Kaplan, G. G., Harris, M. L., & Brant, S. R. (2008) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2007.01780.x · Cited by 400 · see citing works
Rupnik, M., Avesani, V., Janc, M., von Eichel‐Streiber, C., & Delmée, M. (1998) · Journal of Clinical Microbiology · doi:10.1128/jcm.36.8.2240-2247.1998 · Cited by 322 · see citing works
Definition of the single integration site of the pathogenicity locus in Clostridium difficile
Braun, V., Hundsberger, T., Leukel, P., Sauerborn, M., & von Eichel‐Streiber, C. (1996) · Gene · doi:10.1016/s0378-1119(96)00398-8 · Cited by 319 · see citing works
Barbut, F., Mastrantonio, P., Delmée, M., Brazier, J. S., Kuijper, E. J., & Poxton, I. R. (2007) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2007.01824.x · Cited by 295 · see citing works
Spigaglia, P., & Mastrantonio, P. (2002) · Journal of Clinical Microbiology · doi:10.1128/jcm.40.9.3470-3475.2002 · Cited by 277 · see citing works
Inflammatory bowel disease: past, present, and future
Sands, B. E. (2007) · Journal of Gastroenterology · doi:10.1007/s00535-006-1995-7 · Cited by 239 · see citing works
Clostridium difficile toxin expression is inhibited by the novel regulator TcdC
Matamouros, S., England, P., & Dupuy, B. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05739.x · Cited by 236 · see citing works
Curry, S. R., Marsh, J. W., Muto, C. A., O’Leary, M. M., Pasculle, A. W., & Harrison, L. H. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.01599-06 · Cited by 203 · see citing works
Stare, B. G., Rupnik, M., Gerding, D. N., Grabnar, M., & Johnson, S. (2004) · Journal of Medical Microbiology · doi:10.1099/jmm.0.45610-0 · Cited by 164 · see citing works
O’Neill, G. J. (1996) · Anaerobe · doi:10.1006/anae.1996.0028 · Cited by 145 · see citing works
CLOSTRIDIUM DIFFICILE ASSOCIATED DIARRHŒA: A ROLE IN INFLAMMATORY BOWEL DISEASE?
Bolton, R. P., Sherriff, R. J., & Read, A. E. (1980) · The Lancet · doi:10.1016/s0140-6736(80)90940-x · Cited by 144 · see citing works
TRNKA, Y. M., & LaMont, J. T. (1981) · Gastroenterology · doi:10.1016/0016-5085(81)90127-x · Cited by 120 · see citing works
Occurrence of Clostridium difficile toxin during the course of inflammatory bowel disease
Meyers, S., Mayer, L., Bottone, E., Desmond, E., & Janowitz, H. D. (1981) · Gastroenterology · doi:10.1016/0016-5085(81)90128-1 · Cited by 106 · see citing works
Occurrence ofClostridium difficileToxin in Inflammatory Bowel Disease
Rolny, P., Järnerot, G., & Möllby, R. (1983) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365528309181560 · Cited by 103 · see citing works
Drudy, D., Quinn, T., O’Mahony, R., Kyne, L., Gaora, P. Ó., & Fanning, S. (2006) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkl398 · Cited by 96 · see citing works
Clostridium difficile and inflammatory bowel disease.
Greenfield, C., Ramirez, J. R. A., Pounder, R. E., Williams, T. L., Danvers, M., Marper, S. R., & Noone, P. (1983) · Gut · doi:10.1136/gut.24.8.713 · Cited by 85 · see citing works
Genomic Diversity and Relatedness of Bifidobacteria Isolated from a Porcine Cecum
Simpson, P. J., Stanton, C., Fitzgerald, G. F., & Ross, R. P. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.8.2571-2581.2003 · Cited by 84 · see citing works
Self-citationLundeen, S. J., Otterson, M. F., Binion, D. G., Carman, E. T., & Peppard, W. (2007) · Journal of Gastrointestinal Surgery · doi:10.1007/s11605-006-0022-x · Cited by 81 · see citing works
Cartwright, C. P., Stock, F., Beekmann, S. E., Williams, E. C., & Gill, V. J. (1995) · Journal of Clinical Microbiology · doi:10.1128/jcm.33.1.184-187.1995 · Cited by 78 · see citing works
Mutlu, E., Wroe, A. J., Sánchez-Hurtado, K., Brazier, J. S., & Poxton, I. R. (2007) · Journal of Medical Microbiology · doi:10.1099/jmm.0.47176-0 · Cited by 68 · see citing works
How to detect Clostridium difficile variant strains in a routine laboratory
Rupnik, M. (2001) · Clinical Microbiology and Infection · doi:10.1046/j.1198-743x.2001.00290.x · Cited by 59 · see citing works
John, R., & Brazier, J. S. (2005) · Journal of Hospital Infection · doi:10.1016/j.jhin.2005.01.020 · Cited by 52 · see citing works
Variant forms of the binary toxin CDT locus and tcdC gene in Clostridium difficile strains
Stare, B. G., Delmée, M., & Rupnik, M. (2007) · Journal of Medical Microbiology · doi:10.1099/jmm.0.46931-0 · Cited by 52 · see citing works
Sadeghifard, N., Gürtler, V., Beer, M., & Seviour, R. J. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.01179-06 · Cited by 52 · see citing works
Gal, M., Northey, G., & Brazier, J. (2005) · Journal of Hospital Infection · doi:10.1016/j.jhin.2005.01.017 · Cited by 32 · see citing works
Hookman, P., & Barkin, J. S. (2007) · Digestive Diseases and Sciences · doi:10.1007/s10620-006-9450-4 · Cited by 23 · see citing works
Shaaly, A., Tellevik, M. G., Langeland, N., Høiby, E. A., & Jureen, R. (2005) · Journal of Medical Microbiology · doi:10.1099/jmm.0.45912-0 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Kornbluth, A. A., & Sachar, D. B. (2010) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.727 · Cited by 2,019 · see citing works
Current Understanding of Dysbiosis in Disease in Human and Animal Models
DeGruttola, A. K., Low, D., Mizoguchi, A., & Mizoguchi, E. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000750 · Cited by 1,122 · see citing works
Brain-gut-microbe communication in health and disease
Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00094 · Cited by 952 · see citing works
ACG Clinical Guidelines: Prevention, Diagnosis, and Treatment of Clostridioides difficile Infections
Kelly, C. R., Fischer, M., Allegretti, J. R., LaPlante, K. L., Stewart, D. B., Limketkai, B. N., & Stollman, N. (2021) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000001278 · Cited by 615 · see citing works
Phylogenetic Analysis of Dysbiosis in Ulcerative Colitis During Remission
Rajilić-Stojanović, M. D., Shanahan, F., Guarner, F., & de Vos, W. M. (2013) · Inflammatory Bowel Diseases · doi:10.1097/mib.0b013e31827fec6d · Cited by 355 · see citing works
Self-citationClostridium difficile infection: epidemiology, risk factors and management
Ananthakrishnan, A. N. (2010) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2010.190 · Cited by 353 · see citing works
Clostridium difficile and inflammatory bowel disease
Issa, M., Ananthakrishnan, A. N., & Binion, D. G. (2008) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20500 · Cited by 253 · see citing works
Slimy partners: the mucus barrier and gut microbiome in ulcerative colitis
Fang, J. C., Wang, H., Zhou, Y., Zhang, H., Zhou, H., & Zhang, X. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00617-8 · Cited by 242 · see citing works
Vindigni, S. M., Zisman, T. L., Suskind, D. L., & Damman, C. J. (2016) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x16644242 · Cited by 228 · see citing works
Rea, M. C., O’Sullivan, Ó., Shanahan, F., O’Toole, P. W., Stanton, C., Ross, R. P., & Hill, C. (2011) · Journal of Clinical Microbiology · doi:10.1128/jcm.05176-11 · Cited by 224 · see citing works
Self-citationAsymptomatic Clostridium difficile colonization: epidemiology and clinical implications
Furuya‐Kanamori, L., Marquess, J., Yakob, L., Riley, T. V., Paterson, D. L., Foster, N. F., Huber, C. A., & Clements, A. (2015) · BMC Infectious Diseases · doi:10.1186/s12879-015-1258-4 · Cited by 207 · see citing works
Clostridium difficile Infection in Hospitalized Children in the United States
Nylund, C. M., Goudie, A., Garza, J. M., Fairbrother, G., & Cohen, M. B. (2011) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpediatrics.2010.282 · Cited by 202 · see citing works
The involvement of gut microbiota in inflammatory bowel disease pathogenesis: Potential for therapy
Cammarota, G., Ianiro, G., Cianci, R., Bibbò, S., Gasbarrini, A., & Currò, D. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.12.006 · Cited by 180 · see citing works
Fischer, M., Kao, D. H., Kelly, C. R., Kuchipudi, A., Jafri, S., Blumenkehl, M., Rex, D. K., Mellow, M., Kaur, N. J., Sokol, H., et al. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000908 · Cited by 178 · see citing works
Nitzan, O. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i43.7577 · Cited by 174 · see citing works
Inflammatory bowel disease: role of diet, microbiota, life style
Neuman, M. G., & Nanau, R. M. (2011) · Translational research · doi:10.1016/j.trsl.2011.09.001 · Cited by 168 · see citing works
Gut microbiota, the pharmabiotics they produce and host health
Patterson, E., Cryan, J. F., Fitzgerald, G. F., Ross, R. P., Dinan, T. G., & Stanton, C. (2014) · Proceedings of The Nutrition Society · doi:10.1017/s0029665114001426 · Cited by 165 · see citing works
Self-citationSartelli, M., Di Bella, S., McFarland, L. V., Khanna, S., Furuya-Kanamori, L., Abuzeid, N., Abu-Zidan, F. M., Ansaloni, L., Augustin, G., Bala, M., et al. (2019) · World Journal of Emergency Surgery · doi:10.1186/s13017-019-0228-3 · Cited by 159 · 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
Intestinal microbiota: A source of novel biomarkers in inflammatory bowel diseases?
Berry, D., & Reinisch, W. (2013) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2013.03.005 · Cited by 155 · see citing works
Khanna, S., Shin, A., & Kelly, C. P. (2017) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2016.10.024 · Cited by 156 · see citing works
Functional Impacts of the Intestinal Microbiome in the Pathogenesis of Inflammatory Bowel Disease
Li, J. S. Y., Butcher, J., Mack, D. R., & Stintzi, A. P. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000215 · Cited by 153 · see citing works
Clostridium difficile Infection in the Inflammatory Bowel Disease Patient
Berg, A. M., Kelly, C. P., & Farraye, F. A. (2012) · Inflammatory Bowel Diseases · doi:10.1002/ibd.22964 · Cited by 146 · see citing works
Kucharzik, T. F., Taylor, S. A., Allocca, M., Burisch, J. M., Ellul, P., Iacucci, M., Maaser, C., Baldin, P., Bhatnagar, G., Ben‐Horin, S., et al. (2025) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjaf106 · Cited by 140 · see citing works
Clostridium difficile disease: Diagnosis, pathogenesis, and treatment update
Napolitano, L. M., & Edmiston, C. E. (2017) · Surgery · doi:10.1016/j.surg.2017.01.018 · Cited by 132 · see citing works
Antibiotic treatment of acute gastroenteritis in children
Bruzzese, E., Giannattasio, A., & Guarino, A. (2018) · F1000Research · doi:10.12688/f1000research.12328.1 · Cited by 122 · see citing works
“IBD patients have a higher asymptomatic Cd carriage status: as high as 8% compared to a rate of 1% in healthy subjects 40 .”
BackgroundL-arginine metabolism as pivotal interface of mutual host–microbe interactions in the gut
Nüse, B., Holland, T., Rauh, M., Gerlach, R. G., & Mattner, J. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2222961 · Cited by 131 · see citing works
Microbial Induction of Immunity, Inflammation, and Cancer
Greer, J. B., & O’Keefe, S. J. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2010.00168 · Cited by 126 · see citing works
Systematic review: Clostridium difficile and inflammatory bowel disease
Goodhand, J., Alazawi, W., & Rampton, D. S. (2010) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2010.04548.x · Cited by 121 · see citing works
Jen, M., Saxena, S. K., Bottle, A., Aylin, P. P., & Pollok, R. (2011) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2011.04661.x · Cited by 119 · see citing works
Increased Enterococcus faecalis infection is associated with clinically active Crohn disease
Zhou, Y., Chen, H., He, H., Du, Y., Hu, J., Li, Y., Li, Y., Zhou, Y., Wang, H., Chen, Y., et al. (2016) · Medicine · doi:10.1097/md.0000000000005019 · Cited by 117 · see citing works
Xiao, J., Chen, X., Zhan, Q., Zhong, L., Hu, Q., & Zhao, L. (2021) · Ultrasonics Sonochemistry · doi:10.1016/j.ultsonch.2021.105901 · Cited by 100 · see citing works
Navaneethan, U. (2010) · World Journal of Gastroenterology · doi:10.3748/wjg.v16.i39.4892 · Cited by 97 · see citing works
A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease?
Kalischuk, L. D., & Buret, A. G. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00193.2009 · Cited by 95 · see citing works
WSES guidelines for management of Clostridium difficile infection in surgical patients
Sartelli, M., Malangoni, M. A., Abu‐Zidan, F. M., Griffiths, E. A., Bella, S. D., McFarland, L. V., Eltringham, I. J., Shelat, V. G., Velmahos, G. C., Kelly, C. P., et al. (2015) · World Journal of Emergency Surgery · doi:10.1186/s13017-015-0033-6 · Cited by 92 · see citing works
The Role of Bacteria in the Pathogenesis of Inflammatory Bowel Disease
Friswell, M. K., Campbell, B. J., & Rhodes, J. M. (2010) · Gut and Liver · doi:10.5009/gnl.2010.4.3.295 · Cited by 91 · see citing works
Murthy, S. K., Steinhart, A. H., Tinmouth, J., Austin, P. C., Daneman, N., & Nguyen, G. C. (2012) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12073 · Cited by 87 · see citing works
The role of gastrointestinal pathogens in inflammatory bowel disease: a systematic review
Axelrad, J. E., Cadwell, K., Colombel, J., & Shah, S. C. (2021) · Therapeutic Advances in Gastroenterology · doi:10.1177/17562848211004493 · Cited by 86 · see citing works
Ben‐Horin, S., Margalit, M., Bossuyt, P. J., Maul, J., Shapira, Y., Bojic, D., Chermesh, I., Al‐Rifai, A., Schoepfer, A. M., Bosani, M., et al. (2009) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2009.11.001 · Cited by 83 · see citing works
Yanai, H. A., Nguyen, G. C., Yun, L. H., Lebwohl, O., Navaneethan, U., Stone, C. D., Ghazi, L. J., Moayyedi, P., Brooks, J. L., Bernstein, C. N., et al. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21514 · Cited by 80 · see citing works
Impact of Clostridium difficile infection in patients with ulcerative colitis
Kariv, R., Navaneethan, U., Venkatesh, P. G. K., López, R., & Shen, B. (2010) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2010.09.007 · Cited by 80 · see citing works
Gastrointestinal infection as a trigger for inflammatory bowel disease
Mann, E. A., & Saeed, S. A. (2011) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e32834c453e · Cited by 79 · see citing works
Hourigan, S. K., Oliva‐Hemker, M. M., & Hutfless, S. M. (2014) · Digestive Diseases and Sciences · doi:10.1007/s10620-014-3169-4 · Cited by 78 · see citing works
Newman, K. M., Rank, K. M., Vaughn, B. P., & Khoruts, A. (2017) · Gut Microbes · doi:10.1080/19490976.2017.1279377 · Cited by 76 · see citing works
Management of inflammatory bowel disease withClostridium difficileinfection
D’Aoust, J., Battat, R. J., & Bessissow, T. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i27.4986 · Cited by 73 · 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
Clostridium difficile and Pediatric Inflammatory Bowel Disease
Martinelli, M., Strisciuglio, C., Veres, G., Pærregaard, A., Pavić, A. M., Aloi, M., de Carpi, J. M., Levine, A., Turner, D., Pezzo, M. D., et al. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000219 · Cited by 70 · see citing works
Secondary Pouchitis: Those With Identifiable Etiopathogenetic or Triggering Factors
Navaneethan, U., & Shen, B. (2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.530 · Cited by 68 · see citing works
Bacterial Species Associated With Human Inflammatory Bowel Disease and Their Pathogenic Mechanisms
Zhang, L., Liu, F., Xue, J., Lee, S. A., Liu, L., & Riordan, S. M. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.801892 · Cited by 65 · see citing works
Hourigan, S. K., Chirumamilla, S. R., Ross, T. L., Golub, J. E., Rabizadeh, S., Saeed, S. A., Elson, C. O., Kelly, C. P., Carroll, K. C., Oliva‐Hemker, M. M., et al. (2013) · Inflammatory Bowel Diseases · doi:10.1097/01.mib.0000435434.53871.36 · Cited by 64 · see citing works
Chen, T., Zhou, Q., Zhang, D., Jiang, F., Wu, J., Zhou, J., Zheng, X., & Chen, Y. (2018) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjy031 · Cited by 62 · see citing works
Badger, V. O., Ledeboer, N., Graham, M. B., & Edmiston, C. E. (2012) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607112446703 · Cited by 61 · see citing works
Risk Factors and Outcome of PCR-detected Clostridium difficile Infection in Ileal Pouch Patients
Li, Y., Qian, J., Queener, E. Y., & Shen, B. (2013) · Inflammatory Bowel Diseases · doi:10.1097/mib.0b013e318280fcb9 · Cited by 59 · see citing works
Defining Quality Indicators for Best-Practice Management of Inflammatory Bowel Disease in Canada
Nguyen, G. C., Devlin, S. M., Afif, W., Bressler, B. L., Gruchy, S. E., Kaplan, G. G., Oliveira, L., Plamondon, S., Seow, C. H., Williams, C., et al. (2014) · Canadian Journal of Gastroenterology and Hepatology · doi:10.1155/2014/941245 · Cited by 57 · see citing works
Horgan, M., O’Sullivan, Ó., Coffey, A., Fitzgerald, G. F., van Sinderen, D., McAuliffe, O. E., & Ross, R. P. (2010) · Gene · doi:10.1016/j.gene.2010.04.010 · Cited by 55 · see citing works
Self-citationClostridium Difficile and Inflammatory Bowel Disease
Ananthakrishnan, A. N., Issa, M., & Binion, D. G. (2009) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2009.07.003 · Cited by 57 · see citing works
Rao, K. K., & Higgins, P. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000793 · Cited by 54 · see citing works
Du, Z., Hudcovic, T., Mrázek, J., Kozáková, H., Šrůtková, D., Schwarzer, M., Tlaskalová‐Hogenová, H., Kostovčík, M., & Kverka, M. (2015) · Gut Pathogens · doi:10.1186/s13099-015-0080-2 · Cited by 54 · see citing works
Clostridium difficile Infection and Inflammatory Bowel Disease
Reddy, S. S., & Brandt, L. J. (2013) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31828b288a · Cited by 52 · see citing works
Regnault, H., Bourrier, A., Lalande, V., Nion–Larmurier, I., Sokol, H., Seksik, P., Barbut, F., Cosnes, J., & Beaugerie, L. (2014) · Digestive and Liver Disease · doi:10.1016/j.dld.2014.09.003 · Cited by 51 · see citing works
Inflammatory bowel disease—From mechanisms to treatment strategies
Melgar, S., & Shanahan, F. (2010) · Autoimmunity · doi:10.3109/08916931003674709 · Cited by 50 · see citing works
Self-citationClostridium difficile Infection in Special High-Risk Populations
Cózar-Llistó, A., Ramos, A., & Cobo, J. (2016) · Infectious Diseases and Therapy · doi:10.1007/s40121-016-0124-z · Cited by 50 · see citing works
Clostridium difficile Infection and Treatment in the Pediatric Inflammatory Bowel Disease Population
Mezoff, E. A., Mann, E. A., Hart, K. W., Lindsell, C. J., & Cohen, M. B. (2011) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e3181f97209 · Cited by 47 · see citing works
Dalal, R. S., & Allegretti, J. R. (2021) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000739 · Cited by 47 · see citing works
The Colonic Microbiota and Colonic Disease
Shanahan, F. (2012) · Current Gastroenterology Reports · doi:10.1007/s11894-012-0281-5 · Cited by 46 · see citing works
Self-citationArdura, M. I., Toussi, S. S., Siegel, J. D., Lu, Y., Bousvaros, A., & Crandall, W. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001188 · Cited by 45 · see citing works
Law, C. C. Y., Tariq, R., Khanna, S., Murthy, S. K., & McCurdy, J. D. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13972 · Cited by 44 · see citing works
Monaghan, T. M., Robins, A., Knox, A. J., Sewell, H. F., & Mahida, Y. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074452 · Cited by 41 · see citing works
Clostridium Difficile and Inflammatory Bowel Disease
Ananthakrishnan, A. N., Issa, M., & Binion, D. G. (2009) · Medical Clinics of North America · doi:10.1016/j.mcna.2009.08.013 · Cited by 42 · see citing works
The microbiota in inflammatory bowel disease: friend, bystander, and sometime-villain
Shanahan, F. (2012) · Nutrition Reviews · doi:10.1111/j.1753-4887.2012.00502.x · Cited by 42 · see citing works
Self-citationZdzalik, M., Karim, A., Wolski, K., Buda, P., Wójcik, K., Brueggemann, S., Wojciechowski, P., Eick, S., Calander, A., Jonsson, I., et al. (2012) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2012.01005.x · Cited by 41 · see citing works
Masclee, G. M. C., Penders, J., Jonkers, D. M. A. E., Wolffs, P. F. G., & Pierik, M. J. (2013) · Inflammatory Bowel Diseases · doi:10.1097/mib.0b013e318297d222 · Cited by 39 · see citing works
Management of Clostridioides difficile infection in patients with inflammatory bowel disease
Khanna, S. (2020) · Intestinal Research · doi:10.5217/ir.2020.00045 · Cited by 40 · see citing works
Pathogenesis of Clostridium difficile Infection and Its Potential Role in Inflammatory Bowel Disease
Monaghan, T. M., Cockayne, A., & Mahida, Y. R. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000461 · Cited by 38 · see citing works
Zhou, F., Hamza, T., Fleur, A. S., Zhang, Y., Yu, H., Chen, K., Heath, J. E., Chen, Y., Huang, H., & Feng, H. (2018) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izx059 · Cited by 37 · see citing works
Detecting and Treating Clostridium Difficile Infections in Patients with Inflammatory Bowel Disease
Ananthakrishnan, A. N. (2012) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2012.01.003 · Cited by 36 · see citing works
Olteanu, G., Pană, M.-A., Busnatu, Ș., Lupuliasa, D., Neacșu, S. M., Mititelu, M., Musuc, A. M., Ioniță-Mîndrican, C.-B., & Boroghină, S. C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105561 · Cited by 34 · see citing works
Boone, J. H., Goodykoontz, M., Rhodes, S. J., Price, K., Smith, J. R., Gearhart, K. N., Carman, R. J., Kerkering, T. M., Wilkins, T. D., & Lyerly, D. M. (2011) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-011-1477-6 · Cited by 34 · see citing works
Clostridium difficileinfection and inflammatory bowel disease
Musa, S. A., Thomson, S. J., Cowan, M., & Rahman, T. M. (2009) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365520903497098 · Cited by 34 · see citing works
Impact ofClostridium difficileon inflammatory bowel disease
Ananthakrishnan, A. N., & Binion, D. G. (2010) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/egh.10.55 · Cited by 34 · see citing works
Clostridium difficile Infection in Pediatric Inflammatory Bowel Disease
Hourigan, S. K., Sears, C. L., & Oliva‐Hemker, M. M. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000666 · Cited by 34 · see citing works
Clostridium difficile infection in hospitalized patients with inflammatory bowel disease
Maharshak, N., Barzilay, I., Zinger, H., Hod, K., & Dotan, I. (2018) · Medicine · doi:10.1097/md.0000000000009772 · Cited by 34 · see citing works
Burke, D. G., Harrison, M. J., Fleming, C., McCarthy, M. M., Shortt, C., Sulaiman, I., Murphy, D. M., Eustace, J. A., Shanahan, F., Hill, C., et al. (2016) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2016.09.008 · Cited by 31 · see citing works
Self-citationZhou, Y., Mao, L., Yu, J., Lin, Q., Luo, Y., Zhu, X., & Sun, Z. (2019) · BMC Infectious Diseases · doi:10.1186/s12879-019-3841-6 · Cited by 30 · see citing works
Clostridium innocuum infection in hospitalised patients with inflammatory bowel disease
Le, P., Chiu, C., Yeh, P., Pan, Y., & Chiu, C. (2021) · Journal of Infection · doi:10.1016/j.jinf.2021.12.031 · Cited by 30 · see citing works
Boeriu, A. M., Roman, A., Fofiu, C., & Dobru, D. E. (2022) · Pathogens · doi:10.3390/pathogens11070819 · Cited by 29 · see citing works
Clostridium difficile infection in inflammatory bowel disease: challenges in diagnosis and treatment
Tang, Y. M., & Stone, C. D. (2017) · Clinical Journal of Gastroenterology · doi:10.1007/s12328-017-0719-2 · Cited by 29 · see citing works
Inflammatory Diseases of the Gut
Rohr, M., Narasimhulu, C. A., Sharma, D., Doomra, M., Riad, A., Naser, S. A., & Parthasarathy, S. (2018) · Journal of Medicinal Food · doi:10.1089/jmf.2017.0138 · Cited by 29 · see citing works
Choi, Y. J., Kim, J. E., Lee, S. J., Gong, J. E., Son, H. J., Hong, J. T., & Hwang, D. Y. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.650789 · Cited by 28 · see citing works
Sidler, J. A., Battegay, M., Tschudin‐Sutter, S., Widmer, A. F., & Weisser, M. (2014) · Swiss Medical Weekly · doi:10.4414/smw.2014.14009 · Cited by 26 · see citing works
The colonic microflora and probiotic therapy in health and disease
Shanahan, F. (2010) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e328340076f · Cited by 27 · see citing works
Self-citationClostridium difficile Infection in Patients with Inflammatory Bowel Disease
Fu, N., & Wong, T. (2016) · Current Infectious Disease Reports · doi:10.1007/s11908-016-0525-x · Cited by 26 · see citing works
Clostridium difficile infection in patients with inflammatory bowel disease
Czepiel, J., Biesiada, G., Perucki, W. H., & Mach, T. (2014) · Gastroenterology Review · doi:10.5114/pg.2014.43572 · Cited by 26 · see citing works
Kaneko, T., Matsuda, R., Taguri, M., Inamori, M., Ogura, A., Miyajima, E., Tanaka, K., Maeda, S., Kimura, H., & Kunisaki, R. (2011) · Clinics and Research in Hepatology and Gastroenterology · doi:10.1016/j.clinre.2011.02.004 · Cited by 26 · see citing works
Clostridium difficile infection and inflammatory bowel disease
Cojocariu, C., Stanciu, C., Stoica, O. C., Sîngeap, A.-M., Sfarti, C. V., Gîrleanu, I., & Trifan, A. V. (2014) · The Turkish Journal of Gastroenterology · doi:10.5152/tjg.2014.14054 · Cited by 26 · see citing works
Chen, X., Deng, J., Chen, X., Wan, S. S., Wang, Y., & Cao, Q. (2019) · Journal of Digestive Diseases · doi:10.1111/1751-2980.12798 · Cited by 25 · see citing works
Risk factors for the development of Clostridium difficile infection in hospitalized children
Samady, W., Pong, A. L., & Fisher, E. S. (2014) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000000126 · Cited by 24 · see citing works
Zeitz, J., Bissig, M., Barthel, C., Biedermann, L., Scharl, S., Pohl, D., Frei, P., Vavricka, S. R., Fried, M., Rogler, G., et al. (2016) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000000783 · Cited by 24 · see citing works
Cao, Z., Ding, Y., Liu, Z., Liu, M., Wu, H., Zhao, J., Dong, X., & Shang, H. (2023) · Industrial Crops and Products · doi:10.1016/j.indcrop.2023.116318 · Cited by 23 · see citing works
Brace, C., Gloor, G. B., Ropeleski, M. J., Allen‐Vercoe, E., & Petrof, E. O. (2014) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2014.01.020 · Cited by 23 · see citing works
- Authors
- Clayton, E. M., Rea, M. C., Shanahan, F., Quigley, E. M. M., Kiely, B., Hill, C., & Ross, R. P.
- Affiliations
- Teagasc - The Irish Agriculture and Food Development Authority (IE)
- National University of Ireland (IE)
- Alimentary Health (Ireland) (IE)
- Corresponding author
- Shanahan, Fergus
- Venue
- The American Journal of Gastroenterology
- Published
- 2009-03-24
- Volume
- 104
- Issue
- 5
- Pages
- 1162-1169
- ISSN
- 0002-9270 (ISSN-L)
- 1572-0241
- OpenAlex
- W1989402519
- Cited by
- 202
- References
- 35
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 13 · 2023: 11 · 2022: 12 · 2021: 9 · 2020: 10 · 2019: 9 · 2018: 14 · 2017: 15 · 2016: 11 · 2015: 8 · 2014: 19 · 2013: 11 · 2012: 16
- FWCI
- 11.96
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The American Journal of Gastroenterology (publishedVersion)
- PubMed (publishedVersion)
- UCLA - Biblioteca de Ciencias de la Salud (submittedVersion)
- Lenus, The Irish Health Repository (Dr Steevens Hospital Library) (submittedVersion)
- Funders
- University of Pittsburgh
- Health Research Board
- Higher Education Authority
- Science Foundation Ireland
- Division of Mathematical Sciences
- Topics
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- Clostridium difficile, inflammatory bowel disease, ulcerative colitis, Crohn's disease, community-acquired infections, clinical remission, toxinotypes, ribotypes, strain diversity, 16S rRNA gene sequencing, antibiotic susceptibility, nosocomial transmission
- MeSH terms
- Adolescent, Adult, Ambulatory Care, Bacterial Toxins, Carrier State, Clostridium Infections, Colitis, Ulcerative, Crohn Disease, Female, Follow-Up Studies, Humans, Male, Microbial Sensitivity Tests, Middle Aged, Probability, Reference Values, Remission, Spontaneous, Severity of Illness Index, Inflammatory Bowel Diseases, Comorbidity, Incidence, Case-Control Studies, Clostridioides difficile, Age Distribution, Sex Distribution, Young Adult
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
