Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease
Open accessAbstract
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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Spatial niche partitioning of microbial populations can result from mucus from goblet cells and differential oxygen tolerance.
“Spatial niche partitioning of microbial populations can also be a result of mucus from goblet cells 46 and differential oxygen tolerance47.”
From The gut Microbiome in adult and pediatric functional gastrointestinal disorders (2019) · cites this paper as [46]
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BackgroundInfluentialInteraction of gut microbiota with bile acid metabolism and its influence on disease states
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“It is well established that the fecal and intestinal mucosal microbiota of human patients with IBD, particularly ileal Crohn's disease, are highly altered compared to healthy individuals (Swidsinski et al. 2005; Frank et al. 2007; Sokol et al. 2008; Willing et al. 2009).”
BackgroundFrom in vitro to in vivo Models of Bacterial Biofilm-Related Infections
Lebeaux, D., Chauhan, A., Rendueles, O., & Beloin, C. (2013) · Pathogens · doi:10.3390/pathogens2020288 · Cited by 551 · see citing works
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“Modification of gut flora was shown in areas of inflamed gut in IBD patients (Barnich et al., 2003; Darfeuille-Michaud et al., 2004; Martin et al., 2004; Masseret et al., 2001; Ott et al., 2004; Seksik et al., 2003; Swidsinski et al., 2005).”
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“For example, patients with this disease have an increased number of epithelial cell surface– associated bacteria (Swidsinski et al., 2005), suggesting the failure of a mechanism designed to limit direct contact between the epithelium and the microbiota.”
BackgroundAdherent Biofilms in Bacterial Vaginosis
Swidsinski, A. V., Mendling, W., Loening-Baucke, V. A., Ladhoff, A., Swidsinski, S., Hale, L. P., & Lochs, H. H. (2005) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000183594.45524.d2 · Cited by 484 · see citing works
Self-citationRegulatory T Cells in the Control of Host-Microorganism Interactions
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“Most notably, the inflammatory status of the intestine responds to and regulates the proximity and identity of gut microbes closest to the host epithelium (Johansson et al., 2014; Stecher et al., 2007; Swidsinski et al., 2005).”
BackgroundResultInfluentialFight them or feed them: How the intestinal mucus layer manages the gut microbiota
Schroeder, B. O. (2019) · Gastroenterology report · doi:10.1093/gastro/goy052 · Cited by 464 · see citing works
Intestinal microbiota, fecal microbiota transplantation, and inflammatory bowel disease
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“and a significantly higher proportion of the Proteobacteria phylum.(70,71,73,74) Notably, these differences are present even in patients with Crohn’s disease who are treatment-na€ıve, suggesting that intestinal dysbiosis in these patients is not a consequence of therapy, but rather a potential early change in IBD.”
BackgroundPart 1: The Human Gut Microbiome in Health and Disease.
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Molecular analysis of the gut microbiota of identical twins with Crohn's disease
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“Some Bacteroides species have previously been shown to be present in increased levels in persons suffering from IBD (Gophna et al., 2006; Swidsinski et al., 2005), yet animal models have provided conflicting evidence as to which species may cause CD, warranting closer examination.”
BackgroundInteractions of Intestinal Bacteria with Components of the Intestinal Mucus
Sicard, J.-F., Bihan, G. L., Vogeleer, P., Jacques, M., & Harel, J. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00387 · Cited by 455 · see citing works
Gut Microbiota and Inflammation
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“fragilis have also been linked to inflammatory bowel diseases (IBD) [58–60].”
BackgroundSpecificities of the fecal microbiota in inflammatory bowel disease
Sokol, H., Seksik, P., Rigottier‐Gois, L., Lay, C., Lepage, P., Podglajen, I., Marteau, P. R., & Dore, J. M. (2006) · Inflammatory Bowel Diseases · doi:10.1097/01.mib.0000200323.38139.c6 · Cited by 447 · see citing works
Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum / necrophorum
Swidsinski, A. V., Dörffel, Y., Loening-Baucke, V. A., Theissig, F., Rueckert, J.-C., Ismail, M., Rau, W. A., Gaschler, D., Weizenegger, M., Kühn, S., et al. (2009) · Gut · doi:10.1136/gut.2009.191320 · Cited by 441 · see citing works
“Paraffin-embedded caecal biopsies and faecal cylinders (400 each) that were previously investigated in our clinic for the study of mucosal”
MethodSelf-citationImmune Responses to the Microbiota at the Intestinal Mucosal Surface
Duerkop, B. A., Vaishnava, S., & Hooper, L. V. (2009) · Immunity · doi:10.1016/j.immuni.2009.08.009 · Cited by 424 · see citing works
“For example, IBD patients exhibit increased numbers of mucosal surface-associated bacteria (Swidsinski et al., 2005), suggesting a failure of mechanisms that normally sequester microbiota from direct contact with the surface epithelium.”
BackgroundProbiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors
Jones, S. E., & Versalovic, J. A. (2009) · BMC Microbiology · doi:10.1186/1471-2180-9-35 · Cited by 417 · see citing works
“Using non-aqueous fixatives and special techniques, several groups have documented the presence of intestinal biofilms in the mammalian intestine [14-17].”
BackgroundEnterotoxigenic Bacteroides fragilis : a Rogue among Symbiotes
Sears, C. L. (2009) · Clinical Microbiology Reviews · doi:10.1128/cmr.00053-08 · Cited by 412 · see citing works
“The histology of ETBF disease in animals has not identified adherent organisms, but available results are limited by formalin fixation, which can interfere with detection of mucosal adherence in the colon (111).”
BackgroundMénage à trois in the human gut: interactions between host, bacteria and phages
Mirzaei, M. K., & Maurice, C. F. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.30 · Cited by 404 · see citing works
Precision Nutrition and the Microbiome, Part I: Current State of the Science
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“densities of mucosa-associated bacteria were reported in IBD patients [64, 65, 70], and were suspected to play a”
BackgroundGut bacteria in health and disease.
Quigley, E. M. M. (2013) · Europe PMC (PubMed Central) · Cited by 392 · see citing works
Fast food fever: reviewing the impacts of the Western diet on immunity
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“Reduction in Eubacterium is associated with increased incidence of Crohn’s disease [141] while increased presence is associated with both irritable bowel syndrome [142] and inflammatory bowel disease [143].”
BackgroundHold, G. L. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i5.1192 · Cited by 365 · see citing works
Comparative study of the intestinal mucus barrier in normal and inflamed colon
Swidsinski, A. V., Loening-Baucke, V. A., Theissig, F., Engelhardt, H., Bengmark, S., Koch, S., Lochs, H. H., & Dörffel, Y. (2006) · Gut · doi:10.1136/gut.2006.098160 · Cited by 365 · see citing works
Self-citationInteractions between Intestinal Microbiota and Host Immune Response in Inflammatory Bowel Disease
Zhang, M., Sun, K., Wu, Y., Yang, Y., Tso, P., & Wu, Z. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00942 · Cited by 347 · see citing works
“demonstrated increased bacterial adherence to the mucosal surface of IBD patients, indicating a decreased ability to limit direct contact between the epithelium and intestinal microbiota and the potential over-activation of the host immune response (83) (Figure 2).”
BackgroundPhylogenetic 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
Drewes, J. L., White, J. R., Dejea, C. M., Fathi, P., Iyadorai, T., Vadivelu, J., Roslani, A. C., Wick, E. C., Mongodin, E. F., Loke, M. F., et al. (2017) · npj Biofilms and Microbiomes · doi:10.1038/s41522-017-0040-3 · Cited by 335 · see citing works
“In comparison, a range of 13–35% of healthy screening colonoscopy patients have been reported to harbor colonic biofilms, with equivalent percentages of biofilms on the right and left sides.(16,23) Notably, the prevalence of biofilms in the healthy biopsies in the present meta-analysis was lower than expected (6%); ho…”
MethodResultMetabolism Links Bacterial Biofilms and Colon Carcinogenesis
Johnson, C. H., Dejea, C. M., Edler, D., Hoang, L. T., Santidrián, A. F., Felding, B. H., Ivanišević, J., Cho, K., Wick, E. C., Hechenbleikner, E. M., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.04.011 · Cited by 355 · see citing works
“C face and indicate disruption of the normal colon mucous barrier (Probert and Gibson, 2002; Shah and Swiatlo, 2008); in addition, biofilms have been associated with non-malignant pathologies such as inflammatory bowel disease (Swidsinski et al., 2005).”
BackgroundHeimesaat, M. M., Bereswill, S., Fischer, A., Fuchs, D., Struck, D., Niebergall, J., Jahn, H.-K., Dunay, I. R., Moter, A., Gescher, D. M., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.12.8785 · Cited by 345 · see citing works
“Intestinal bacteria trigger large bowel inflammation in IBD (2–7) and graft-vs-host disease (GvHD) after bone marrow transplantation (8, 9).”
BackgroundInfluentialSwidsinski, A. V., Mendling, W., Loening-Baucke, V. A., Swidsinski, S., Dörffel, Y., Scholze, J., Lochs, H. H., & Verstraelen, H. (2007) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.06.039 · Cited by 337 · see citing works
Self-citationScanlan, P. D., Shanahan, F., O'Mahony, C., & Marchesi, J. R. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.00312-06 · Cited by 330 · see citing works
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Gut microbiota role in irritable bowel syndrome: New therapeutic strategies
Distrutti, E., Monaldi, L., Ricci, P., & Fiorucci, S. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i7.2219 · Cited by 320 · see citing works
Role of the microbiota in inflammatory bowel diseases
Nagalingam, N. A., & Lynch, S. V. (2012) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21866 · Cited by 315 · see citing works
Antimicrobial Defense of the Intestine
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Nod2 is essential for temporal development of intestinal microbial communities
Rehman, A., Sina, C., Gavrilova, O., Häsler, R., Ott, S. J., Baines, J. F., Schreiber, S., & Rosenstiel, P. C. (2011) · Gut · doi:10.1136/gut.2010.216259 · Cited by 316 · see citing works
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“Indeed, patients with inflammatory bowel disease exhibit increased numbers of microbes associated with the gut mucosa [45–49], and innate immune defects have been shown to exist in patients with Crohn’s disease [50].”
Mucins and Their Role in Shaping the Functions of Mucus Barriers
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“In health, mucus appears to play an important role in suppressing virulence of these opportunistic pathogens and in promoting their coexistence as part of a stable microbiota (Swidsinski et al. 2005).”
Chronic wounds and the medical biofilm paradigm
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The intestinal microbiota and chronic disorders of the gut
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“Patients with IBD were shown to have twice the concentration of mucosal Bacteroides fragilis biofilm compared with controls, the concentration of which was modified by antimicrobial therapy”
BackgroundBacArena: Individual-based metabolic modeling of heterogeneous microbes in complex communities
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Commensal and Pathogenic Escherichia coli Metabolism in the Gut
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The Genotypic View of Social Interactions in Microbial Communities
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Microbiota-derived lantibiotic restores resistance against vancomycin-resistant Enterococcus
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Interplay Between Exercise and Gut Microbiome in the Context of Human Health and Performance
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Role of antibiotics for treatment of inflammatory bowel disease
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Cultivable bacterial diversity from the human colon
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“Bacteroides spp. may also be particularly dominant in mucosal biofilms from ulcerative colitis patients (Swidsinski et al. 2005).”
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Gastrointestinal biofilms in health and disease
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Long‐term monitoring of the human intestinal microbiota composition
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“Data inappropriate for analysis (n = 4) [20, 21, 22, 23] Animal experiments excluded (n = 21)”
BackgroundMethodInfluentialGastrointestinal microbiota in irritable bowel syndrome: present state and perspectives
Salonen, A., de Vos, W. M., & Palva, A. (2010) · Microbiology · doi:10.1099/mic.0.043257-0 · Cited by 264 · see citing works
“A fluorescence in situ hybridization (FISH) study showed unsubtyped IBS patients to harbour slightly more total bacteria and significantly more members of Clostridium cluster XIVa than the HCs (Swidsinski et al., 2005).”
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- Authors
- Swidsinski, A., Weber, J., Loening-Baucke, V., Hale, L. P., & Lochs, H.
- Affiliations
- Humboldt-Universität zu Berlin (DE)
- Duke Medical Center (US)
- 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
- 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
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Epidemiology › 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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