Cited by 894Gut microbiota and healthInflammatory Bowel DiseaseMicroscopic Colitis

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Spatial Organization and Composition of the Mucosal Flora in Patients with Inflammatory Bowel Disease

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Swidsinski, Alexander, Weber, Jutta, Loening-Baucke, Vera, Hale, Laura P., Lochs, Herbert·2005·Journal of Clinical Microbiology

DOI 10.1128/jcm.43.7.3380-3389.2005PMC PMC1169142

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Abstract

The composition and spatial organization of the mucosal flora in biopsy specimens from patients with inflammatory bowel disease (IBD; either Crohn's disease or ulcerative colitis), self-limiting colitis, irritable-bowel syndrome (IBS), and healthy controls were investigated by using a broad range of fluorescent bacterial group-specific rRNA-targeted oligonucleotide probes. Each group included 20 subjects. Ten patients who had IBD and who were being treated with antibiotics were also studied. Use of nonaqueous Carnoy fixative to preserve the mucus layer was crucial for detection of bacteria adherent to the mucosal surface (mucosal bacteria). No biofilm was detectable in formalin-fixed biopsy specimens. Mucosal bacteria were found at concentrations greater than 10 9 /ml in 90 to 95% of IBD patients, 95% of patients with self-limiting colitis, 65% of IBS patients, and 35% of healthy controls. The mean density of the mucosal biofilm was 2 powers higher in IBD patients than in patients with IBS or controls, and bacteria were mostly adherent. Bacteroides fragilis was responsible for >60% of the biofilm mass in patients with IBD but for only 30% of the biofilm mass in patients with self-limiting colitis and <15% of the biofilm mass in patients with IBS. In contrast, bacteria which positively hybridized with the probe specific for Eubacterium rectale - Clostridium coccoides accounted for >40% of the biofilm in IBS patients but for <15% of the biofilm in IBD patients. In patients treated with (5-ASA) or antibiotics, the biofilm could be detected with 4,6-diamidino-2-phenylindole but did not hybridize with fluorescence in situ hybridization probes. A Bacteroides fragilis biofilm is the main feature of IBD. This was not previously recognized due to a lack of appropriate tissue fixation. Both 5-ASA and antibiotics suppress but do not eliminate the adherent biofilm.

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BackgroundResult
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BackgroundResultInfluential
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Method
Increased Enterococcus faecalis infection is associated with clinically active Crohn disease
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Background
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Result
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BackgroundInfluentialSelf-citation
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Background
Recent developments in the pathophysiology of irritable bowel syndrome
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Result
Pathogenesis of mucosal biofilm infections: challenges and progress
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Background
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Background
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“Additional primers were used to differentiate species that showed inconclusive results as previously described [42].”
Background
Altered Fecal Microbiota in Paediatric Inflammatory Bowel Disease
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“2018  16S rRNA sequencing  Mucosal biopsies samples  14 UC  14 Non-IBD (Controls)  (6/8 )  (8/6)  45 (17-67)  59 (41-73) N/A - Cloacibacterium, Neisseria genus, Tissierellaceae family, (↑inflammed site UC compared to noninflamed site UC) - Prevotella, Eubacterium, Neisseria, Leptotrichia, Bilophila, Desulfovib…”
BackgroundInfluential
Microbial host interactions in IBD: Implications for pathogenesis and therapy
Sartor, R. B., & Muehlbauer, M. (2007) · Current Gastroenterology Reports · doi:10.1007/s11894-007-0066-4 · Cited by 106
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“For example, increased levels of Veillonella are associated with higher levels of gut inflammation and the development of colitis and Crohn’s disease [26,27].”
Background
Exploiting a host-commensal interaction to promote intestinal barrier function and enteric pathogen tolerance
Pedicord, V. A., Lockhart, A. A. K., Rangan, K. J., Craig, J. W., Loschko, J., Rogoz, A., Hang, H. C., & Mucida, D. (2016) · Science Immunology · doi:10.1126/sciimmunol.aai7732 · Cited by 99
“To visualize bacterial segregation from the intestinal epithelium, 16S rRNA FISH was performed with a universal probe (EUB388, Cy3-GCTGCCTCCCGTAGGAGT-Cy3) on sections fixed with Methacarn solution as described previously (69, 70).”
Method
Bacterial protein signals are associated with Crohn’s disease
Juste, C., Kreil, D. P., Beauvallet, C., Guillot, A., Vaca, S., Carapito, C., Mondot, S., Sykacek, P., Sokol, H., Blon, F., et al. (2014) · Gut · doi:10.1136/gutjnl-2012-303786 · Cited by 100
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“Biofilms of bacteria related to potential AcH accumulators on the colorectal mucosa have been confirmed by different methods 21,48–52 .”
Influential
The biofilm mode of life boosts the anti-inflammatory properties ofLactobacillus
Rieu, A., Aoudia, N., Jégo, G., Chluba, J., Yousfi, N., Briandet, R., Deschamps, J., Gasquet, B., Monedero, V., Garrido, C., et al. (2014) · Cellular Microbiology · doi:10.1111/cmi.12331 · Cited by 101
“The mucosal bacteria found in patients with IBD can thus be regarded as an intestinal biofilm (Swidsinski et al., 2005).”
Background
Characterization of the Gastrointestinal Microbiota in Health and Inflammatory Bowel Disease
Cruz, P. P. D., Prideaux, L., Wagner, J., Ng, S. C., McSweeney, C. S., Kirkwood, C. D., Morrison, M., & Kamm, M. A. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21751 · Cited by 97
“However, recent pyrosequencing studies suggest that the FAM of UC patients in remission is similar to that of healthy controls.91 CD appears to be associated with a reduction in the diversity of the phylum Firmicutes, particularly the Clostridium leptum subgroup, in both the FAM82,127,131,142 and MAM.3,145,149 In part…”
Background
Comprehensive Postmortem Analyses of Intestinal Microbiota Changes and Bacterial Translocation in Human Flora Associated Mice
Heimesaat, M. M., Boelke, S., Fischer, A., Haag, L.-M., Loddenkemper, C., Kühl, A. A., Göbel, U. B., & Bereswill, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040758 · Cited by 98
“ulcerative colitis, Graft-versus-host disease, liver injury, portal vein obstruction, prolonged enteral feeding, or under conditions of reduced bowel motility [17,18,19,20,21,22,23,24,25].”
Background
Intestinal Bacteroides species associated with coeliac disease
Sánchez, E., Donat, E., Ribes‐Koninckx, C., Calabuig, M., & Sanz, Y. (2010) · Journal of Clinical Pathology · doi:10.1136/jcp.2010.076950 · Cited by 95
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
“The intestinal microflora of patients with CD also has a higher prominence of potentially detrimental bacteria such as Bacteroides vulgatus (41, 104, 124), which have been shown to induce intestinal inflammation in animal models of IBD (88, 101, 102).”
Background
Characterization of MabA, a modulator ofLactobacillus rhamnosusGG adhesion and biofilm formation
Vélez, M. P., Petrova, M., Lebeer, S., Verhoeven, T. L. A., Claes, I. J. J., Lambrichts, I., Tynkkynen, S., Vanderleyden, J., & Keersmaecker, S. C. J. D. (2010) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2010.00680.x · Cited by 97
“multispecies microcolony formation in healthy individuals (Macfarlane et al., 2004; Swidsinski et al., 2005).”
Background
Replication of Colonic Crohn's Disease Mucosal Escherichia coli Isolates within Macrophages and Their Susceptibility to Antibiotics
Subramanian, S., Roberts, C. L., Hart, C. A., Martin, H., Edwards, S. W., Rhodes, J. M., & Campbell, B. J. (2007) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00375-07 · Cited by 97
“CD patients commonly have circulating antibodies against clostridial flagellin (31) and have a greater proportion of Bacteroides fragilis in their mucosal biofilm (70).”
Background
Effects of the cathelicidin LL-37 on intestinal epithelial barrier integrity
Otte, J., Zdebik, A., Brand, S., Chromik, A. M., Strauß, S., Schmitz, F., Steinstraesser, L., & Schmidt, W. E. (2009) · Regulatory Peptides · doi:10.1016/j.regpep.2009.03.009 · Cited by 94
Lactulose and Lactobacillus plantarum, a Potential Complementary Synbiotic To Control Postweaning Colibacillosis in Piglets
Guerra-Ordaz, A. A., González‐Ortiz, G., Ragione, R. M. L., Woodward, M. J., Collins, J. W., Pérez, J. F., & Martín-Orúe, S. M. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.00770-14 · Cited by 95
“sections from the ileum were removed, opened longitudinally, and fixed by immersion in Carnoy solution as previously described (20).”
Method
The Dysregulation of Polyamine Metabolism in Colorectal Cancer Is Associated with Overexpression of c‐Myc and C/EBPβ rather than Enterotoxigenic Bacteroides fragilis Infection
Snezhkina, A. V., Krasnov, G. S., Lipatova, A. V., Садритдинова, А. Ф., Kardymon, O. L., Fedorova, M., Melnikova, N. V., Stepanov, O. A., Zaretsky, A. R., Каприн, А. Д., et al. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/2353560 · Cited by 94
“fragilis that produce enterotoxin are associated with the development of inflammatory diarrheal disease in both children and adults [41, 42], IBD [43], and colitis [44], thereby contributing to chronic inflammation and onset of colon tumors.”
Background
Mechanisms 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 97
The complex metabolism of trimethylamine in humans: endogenous and exogenous sources
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Similarity and Divergence among Adherent-Invasive Escherichia coli and Extraintestinal Pathogenic E. coli Strains
Martínez-Medina, M., Mora, A., Blanco, M., López, C., Alonso, M. P., Bonacorsi, S., Nicolas-Chanoine, M.-H., Darfeuille–Michaud, A., Garcia-Gil, L. J., & Blanco, J. (2009) · Journal of Clinical Microbiology · doi:10.1128/jcm.01484-09 · Cited by 93
“In part, this suggestion was based on the higher abundance of this bacterium in CD patients than in control subjects (4, 10, 20, 23, 28, 29, 32, 41, 48, 51).”
Background
Macropinocytosis in Shiga toxin 1 uptake by human intestinal epithelial cells and transcellular transcytosis
Malyukova, I. V., Murray, K. F., Zhu, C., Boedeker, E. C., Kane, A. V., Patterson, K., Peterson, J. R., Donowitz, M., & Kovbasnjuk, O. N. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90347.2008 · Cited by 94
Relationship between mucosa-associated gut microbiota and human diseases
Juge, N. (2022) · Biochemical Society Transactions · doi:10.1042/bst20201201 · Cited by 98
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
“sterile but that there is a marked increase in bacteria in Crohn’s disease, and to a lesser extent in ulcerative colitis (UC).(7,8) E.”
Microbial biofilms and gastrointestinal diseases
von Rosenvinge, E. C., O’May, G. A., Macfarlane, S., Macfarlane, G. T., & Shirtliff, M. E. (2012) · Pathogens and Disease · doi:10.1111/2049-632x.12020 · Cited by 91
“, 2003), and irritable bowel syndrome (IBS; Swidsinski et al., 2005).”
Influential
Know your neighbor: Microbiota and host epithelial cells interact locally to control intestinal function and physiology
Sommer, F., & Bäckhed, F. (2016) · BioEssays · doi:10.1002/bies.201500151 · Cited by 96
Species Level Description of the Human Ileal Bacterial Microbiota
Villmones, H. C., Haug, E. S., Ulvestad, E., Grude, N., Stenstad, T., Halland, A., & Kommedal, Ø. (2018) · Scientific Reports · doi:10.1038/s41598-018-23198-5 · Cited by 91
Secondary causes of inflammatory bowel diseases
Ghouri, Y. A., Tahan, V., & Shen, B. (2020) · World Journal of Gastroenterology · doi:10.3748/wjg.v26.i28.3998 · Cited by 94
Bacterial biofilms in the human body: prevalence and impacts on health and disease
Perry, E. K., & Tan, M. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1237164 · Cited by 107
“Frontiers in Cellular and Infection Microbiology 08 (Swidsinski et al., 2005b; Drewes et al., 2017).”
BackgroundInfluential
Mucus, commensals, and the immune system
Zhao, Q. S., & Maynard, C. L. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2041342 · Cited by 91
Insights into inflammatory bowel disease using Toxoplasma gondii as an infectious trigger
Egan, C. E., Cohen, S. B., & Denkers, E. (2011) · Immunology and Cell Biology · doi:10.1038/icb.2011.93 · Cited by 88
Slc26a3 deficiency is associated with loss of colonic HCO 3− secretion, absence of a firm mucus layer and barrier impairment in mice
Xiao, F., Yu, Q., Li, J., Johansson, M., Singh, A. K., Xia, W., Riederer, B., Engelhardt, R., Montrose, M. H., Soleimani, M., et al. (2013) · Acta Physiologica · doi:10.1111/apha.12220 · Cited by 88
“Recent investigations demonstrated the high expression of this gene (Talbot & Lytle 2010, Xiao et al. 2012a) in the mid-distal colon, where it absorbs Cl in exchange for HCO3 .”
Background
High-throughput sequencing provides insights into oral microbiota dysbiosis in association with inflammatory bowel disease
Qi, Y., Zang, S., Wei, J., Yu, H.-C., Yang, Z., Wu, H., Kang, Y., Tao, H., Yang, M., Jin, L., et al. (2020) · Genomics · doi:10.1016/j.ygeno.2020.09.063 · Cited by 88
Microbiome-mediated bile acid modification: Role in intestinal drug absorption and metabolism
Enright, E. F., Griffin, B. T., Gahan, C. G. M., & Joyce, S. A. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.04.009 · Cited by 91
Periodontal connection with intestinal inflammation: Microbiological and immunological mechanisms
Kitamoto, S., & Kamada, N. (2022) · Periodontology 2000 · doi:10.1111/prd.12424 · Cited by 91
Spatial organisation of microbiota in quiescent adenoiditis and tonsillitis
Swidsinski, A. V., Göktas, Ö., Bessler, C., Loening-Baucke, V. A., Hale, L. P., Andree, H., Weizenegger, M., Hölzl, M., Scherer, H. H., & Lochs, H. H. (2006) · Journal of Clinical Pathology · doi:10.1136/jcp.2006.037309 · Cited by 86
Self-citation
Anti-Inflammatory Implications of the Microbial Transformation of Dietary Phenolic Compounds
Russell, W. R., Scobbie, L., Chesson, A., Richardson, A. J., Stewart, C. S., Duncan, S. H., Drew, J. E., & Duthie, G. G. (2008) · Nutrition and Cancer · doi:10.1080/01635580801987498 · Cited by 86
“Despite the obvious association between the colonic environment with inflammation ( 5 , 6 , 7 ), very few studies have addressed the involvement of gut bacteria and their ability to modulate inflammatory compounds derived from “non-nutritive” phytochemicals consumed in the diet.”
Background
Epithelial CaSR deficiency alters intestinal integrity and promotes proinflammatory immune responses
Cheng, S. X., Lightfoot, Y. L., Yang, T., Zadeh, M., Tang, L., Sahay, B., Wang, G. P., Owen, J. L., & Mohamadzadeh, M. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.05.007 · Cited by 85
“Indeed, depletion of Clostridia has been consistently associated with chronic inflammation in patients with IBD [62–65] and atopy [66], whereas Deferribacteraceae was shown to correlate with the level of inflammatory responses in C.”
Gut mucosal-associated microbiota better discloses inflammatory bowel disease differential patterns than faecal microbiota
Altomare, A., Putignani, L., CHIERICO, F. D., Cocca, S., Angeletti, S., Ciccozzi, M., Tripiciano, C., Piccola, B. D., Cicala, M., & Guarino, M. P. L. (2018) · Digestive and Liver Disease · doi:10.1016/j.dld.2018.11.021 · Cited by 86
Modulation of Gut Mucosal Microbiota As a Mechanism of Probiotics-Based Adjunctive Therapy for Ulcerative Colitis
Chen, P., Xu, H., Tang, H., Zhao, F., Yang, C., Kwok, L., Cong, C., Wu, Y., Zhang, W., Zhou, X., et al. (2019) · Microbial Biotechnology · doi:10.1111/1751-7915.13661 · Cited by 85
“On the other hand, a previous study also reported that mesalazine treatment could reduce the mucosal bacteria of patients with UC (Swidsinski et al., 2005).”
BackgroundResult
Inflammatory Bowel Disease and Colon Cancer
Jawad, N., Direkze, N. C., & Leedham, S. J. (2011) · Recent results in cancer research/Recent Results in Cancer Research · doi:10.1007/978-3-642-03503-6_6 · Cited by 84
“In addition to this 5-ASA’s scavenge oxygen free radicals and have an antimicrobial action (Swidsinski et al. 2005).”
Background
A molecular revolution in the study of intestinal microflora
Furrie, E. (2006) · Gut · doi:10.1136/gut.2005.081695 · Cited by 89
Helicobacter typhlonius and Helicobacter rodentium differentially affect the severity of colon inflammation and inflammation-associated neoplasia in IL10-deficient mice.
Chichlowski, M., Sharp, J. M., Vanderford, D. A., Myles, M. H., & Hale, L. P. (2008) · PubMed Central · Cited by 83
Self-citation
Evidence for the involvement of infectious agents in the pathogenesis of Crohn’s disease
Hertogh, G. D. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.845 · Cited by 82
Reduced diversity and increased virulence-gene carriage in intestinal enterobacteria of coeliac children
Sánchez, E., Nadal, I., Donat, E., Ribes‐Koninckx, C., Calabuig, M., & Sanz, Y. (2008) · BMC Gastroenterology · doi:10.1186/1471-230x-8-50 · Cited by 83
“This phenomenon has been named "dysbiosis" [4,5].”
Virulence factors ofEnterococcusstrains isolated from patients with inflammatory bowel disease
Golińska, E. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i23.3562 · Cited by 83
Micromanagement in the gut: microenvironmental factors govern colon mucosal biofilm structure and functionality
Weirdt, R. D., & de Wiele, T. V. (2015) · npj Biofilms and Microbiomes · doi:10.1038/npjbiofilms.2015.26 · Cited by 86
Commensal inter-bacterial interactions shaping the microbiota
Kern, L., Abdeen, S. K., Kolodziejczyk, A. A., & Elinav, E. (2021) · Current Opinion in Microbiology · doi:10.1016/j.mib.2021.07.011 · Cited by 82
Potential Role of Biofilm Formation in the Development of Digestive Tract Cancer With Special Reference to Helicobacter pylori Infection
Rizzato, C., Torres, J., Kasamatsu, E., Camorlinga‐Ponce, M., Bravo, M. M., Canzian, F., & Kato, I. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00846 · Cited by 83
Microbiome Composition in Both Wild-Type and Disease Model Mice Is Heavily Influenced by Mouse Facility
Parker, K. D., Albeke, S. E., Gigley, J. P., Goldstein, A. M., & Ward, N. L. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01598 · Cited by 82
Antibacterial and antibiofilm effects of α-humulene against Bacteroides fragilis
Jang, H.-I., Rhee, K., & Eom, Y. (2020) · Canadian Journal of Microbiology · doi:10.1139/cjm-2020-0004 · Cited by 80
“B. fragilis accounted for 48 more than 60% of the biofilms in IBD patients (Swidsinski et al. 2005).”
Background
Epithelial Cells Augment Barrier Function via Activation of the Toll-Like Receptor 2/Phosphatidylinositol 3-Kinase Pathway upon Recognition of Salmonella enterica Serovar Typhimurium Curli Fibrils in the Gut
Oppong, G. O., Rapsinski, G. J., Newman, T., Nishimori, J. H., Biesecker, S. G., & Tükel, Ç. (2012) · Infection and Immunity · doi:10.1128/iai.00453-12 · Cited by 82
Olfactomedin-4 is a glycoprotein secreted into mucus in active IBD
Gersemann, M., Becker, S., Nuding, S., Antoni, L., Ott, G., Fritz, P., Oue, N., Yasui, W., Wehkamp, J., & Stange, E. F. (2011) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2011.09.013 · Cited by 80
Impact of the gut microbiome on mucosal inflammation
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Elevated lipopolysaccharide in the colon evokes intestinal inflammation, aggravated in immune modulator-impaired mice
Im, E., Riegler, F. M., Pothoulakis, C., & Rhee, S. H. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00120.2012 · Cited by 79
“Similarly, TLR4 was suggested to be strongly upregulated in IBD patients (2), and a TLR4 antagonist was shown to ameliorate mouse experimental colitis (12).”
BackgroundInfluential

Authors: Swidsinski, A., Weber, J., Loening-Baucke, V., Hale, L. P., & Lochs, H.
Affiliations: Humboldt-Universität zu Berlin (DE)
Duke Medical Center (US)
ORCID: Swidsinski, Alexander
Hale, Laura P.
Venue: Journal of Clinical Microbiology
Publisher: American Society for Microbiology
Published: 2005-07
Volume: 43
Issue: 7
Pages: 3380-3389
ISSN: 0095-1137 (ISSN-L)
1098-660X
DOI: 10.1128/jcm.43.7.3380-3389.2005
PMC: PMC1169142
OpenAlex: W2097177097
Cited by: 894
References: 36
Citations by year: 2026: 15 · 2025: 27 · 2024: 45 · 2023: 47 · 2022: 59 · 2021: 47 · 2020: 50 · 2019: 54 · 2018: 46 · 2017: 35 · 2016: 47 · 2015: 49 · 2014: 41 · 2013: 43 · 2012: 44
FWCI: 12.71
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Clinical Microbiology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Eli and Edythe Broad Foundation
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
Health Sciences › Medicine › Gastroenterology › Microscopic Colitis
Keywords: inflammatory bowel disease, Crohn's disease, ulcerative colitis, Bacteroides fragilis, irritable bowel syndrome, 5-aminosalicylic acid, antibiotic therapy, bacterial adhesion, fluorescence in situ hybridization, rRNA-targeted oligonucleotide probes
MeSH terms: Adult, Bacteria, Bacteroides fragilis, Biopsy, Colitis, Ulcerative, Crohn Disease, Female, Humans, Intestinal Mucosa, Male, Middle Aged, Colon, Sigmoid, In Situ Hybridization, Fluorescence, Ecosystem, Biofilms

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Spatial Organization and Composition of the Mucosal Flora in Patients with Inflammatory Bowel Disease

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