The DOI matches its Crossref record; 62 of the 62 references it cites were found in a registry or an index.
Bowel Biofilms: Tipping Points between a Healthy and Compromised Gut?
Open accessAbstract
Bacterial communities are known to impact human health and disease. Mixed species biofilms, mostly pathogenic in nature, have been observed in dental and gastric infections as well as in intestinal diseases, chronic gut wounds and colon cancer. Apart from the appendix, the presence of thick polymicrobial biofilms in the healthy gut mucosa is still debated. Polymicrobial biofilms containing potential pathogens appear to be an early-warning signal of developing disease and can be regarded as a tipping point between a healthy and a diseased state of the gut mucosa. Key biofilm-forming pathogens and associated molecules hold promise as biomarkers. Criteria to distinguish microcolonies from biofilms are crucial to provide clarity when reporting biofilm-related phenomena in health and disease in the gut.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Citations
Cites
Diversity of the Human Intestinal Microbial Flora
Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E., & Relman, D. A. (2005) · Science · doi:10.1126/science.1110591 · Cited by 7,913
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995) · Annual Review of Microbiology · doi:10.1146/annurev.mi.49.100195.003431 · Cited by 4,921
Early-warning signals for critical transitions
Scheffer, M., Bascompte, J., Brock, W. A., Brovkin, V., Carpenter, S. R., Dakos, V., Held, H., van Nes, E. H., Rietkerk, M., & Sugihara, G. (2009) · Nature · doi:10.1038/nature08227 · Cited by 4,854
Biofilms as Complex Differentiated Communities
Stoodley, P., Sauer, K., Davies, D. G., & Costerton, J. W. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160705 · Cited by 3,151
Commensal Host-Bacterial Relationships in the Gut
Hooper, L. V., & Gordon, J. I. (2001) · Science · doi:10.1126/science.1058709 · Cited by 2,362
Johansson, M., Larsson, J. M. H., & Hansson, G. C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006451107 · Cited by 1,535
Electron transfer in syntrophic communities of anaerobic bacteria and archaea
Stams, A. J. M., & Plugge, C. M. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2166 · Cited by 1,441
Mucosal flora in inflammatory bowel disease
Swidsinski, A. V., Ladhoff, A., Pernthaler, A., Swidsinski, S., Loening-Baucke, V. A., Ortner, M., Weber, J., Hoffmann, U., Schreiber, S., Dietel, M., et al. (2002) · Gastroenterology · doi:10.1053/gast.2002.30294 · Cited by 1,344
How informative is the mouse for human gut microbiota research?
Nguyen, T. L. A., Vieira-Silva, S., Liston, A., & Raes, J. (2015) · Disease Models & Mechanisms · doi:10.1242/dmm.017400 · Cited by 1,334
The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
Morris, J., Lenski, R. E., & Zinser, E. R. (2012) · mBio · doi:10.1128/mbio.00036-12 · Cited by 1,231
Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria
Dejea, C. M., Fathi, P., Craig, J. M., Boleij, A., Taddese, R., Geis, A. L., Wu, X., DeStefano Shields, C. E., Hechenbleikner, E. M., Huso, D. L., et al. (2018) · Science · doi:10.1126/science.aah3648 · Cited by 1,105
Johansson, M. E. V., Gustafsson, J. K., Holmén-Larsson, J., Jabbar, K. S., Xia, L., Xu, H., Ghishan, F. K., Carvalho, F. A., Gewirtz, A. T., Sjövall, H., et al. (2014) · Gut · doi:10.1136/gutjnl-2012-303207 · Cited by 1,004
Swidsinski, A., Weber, J., Loening-Baucke, V., Hale, L. P., & Lochs, H. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.7.3380-3389.2005 · Cited by 894
Understanding the effects of diet on bacterial metabolism in the large intestine
Louis, P., Scott, K. P., Duncan, S. H., & Flint, H. J. (2007) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2007.03322.x · Cited by 775
Microbiota organization is a distinct feature of proximal colorectal cancers
Dejea, C. M., Wick, E. C., Hechenbleikner, E. M., White, J. R., Mark Welch, J. L., Rossetti, B. J., Peterson, S. N., Snesrud, E. C., Borisy, G. G., Lazarev, M., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1406199111 · Cited by 700
Gut microbiota utilize immunoglobulin A for mucosal colonization
Donaldson, G. P., Ladinsky, M. S., Yu, K. B., Sanders, J. G., Yoo, B. B., Chou, W., Conner, M. E., Earl, A. M., Knight, R. D., Björkman, P. J., et al. (2018) · Science · doi:10.1126/science.aaq0926 · Cited by 650
Mouse models for human intestinal microbiota research: a critical evaluation
Hugenholtz, F., & de Vos, W. M. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2693-8 · Cited by 610
Interactions in multispecies biofilms: do they actually matter?
Burmølle, M., Ren, D., Bjarnsholt, T., & Sørensen, S. J. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2013.12.004 · Cited by 580
Normalization of host intestinal mucus layers requires long-term microbial colonization
Johansson, M. E. V., Jakobsson, H. E., Holmén-Larsson, J., Schütte, A., Ermund, A., Rodríguez-Piñeiro, A. M., Arike, L., Wising, C., Svensson, F., Bäckhed, F., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.10.007 · Cited by 549
The oral microbiome in health and disease and the potential impact on personalized dental medicine
Zarco, M., Vess, T., & Ginsburg, G. (2011) · Oral Diseases · doi:10.1111/j.1601-0825.2011.01851.x · Cited by 521
The role of biofilms as environmental reservoirs of antibiotic resistance
Balcázar, J. L., Subirats, J., & Borrego, C. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01216 · Cited by 519
Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease
Hoarau, G., Mukherjee, P. K., Gower‐Rousseau, C., Hager, C. L., Chandra, J., Retuerto, M. A., Neut, C., Vermeire, S., Clemente, J. C., Colombel, J., et al. (2016) · mBio · doi:10.1128/mbio.01250-16 · Cited by 499
The oral microbiota: Living with a permanent guest
Avila, M., Ojcius, D. M., & Yilmaz, Ö. (2009) · DNA and Cell Biology · doi:10.1089/dna.2009.0874 · Cited by 482
Sonnenburg, J. L., Angenent, L. T., & Gordon, J. I. (2004) · Nature Immunology · doi:10.1038/ni1079 · Cited by 417
High-avidity IgA protects the intestine by enchaining growing bacteria
Moor, K., Diard, M., Sellin, M. E., Felmy, B., Wotzka, S. Y., Toska, A., Bakkeren, E., Arnoldini, M., Bansept, F., Co, A. D., et al. (2017) · Nature · doi:10.1038/nature22058 · Cited by 411
Biofilms in the large bowel suggest an apparent function of the human vermiform appendix
Randal Bollinger, R., Barbas, A. S., Bush, E. L., Lin, S. S., & Parker, W. (2007) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2007.08.032 · Cited by 373
Oral Biofilms: Emerging Concepts in Microbial Ecology
Filoche, S. K., Wong, L., & Sissons, C. H. (2009) · Journal of Dental Research · doi:10.1177/0022034509351812 · Cited by 370
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
Metabolism 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
Tipping elements in the human intestinal ecosystem
Lahti, L., Salojärvi, J., Salonen, A., Scheffer, M., & de Vos, W. M. (2014) · Nature Communications · doi:10.1038/ncomms5344 · Cited by 336
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
Commensal and Pathogenic Escherichia coli Metabolism in the Gut
Conway, T., & Cohen, P. S. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mbp-0006-2014 · Cited by 323
Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice
Planer, J. D., Peng, Y., Kau, A. L., Blanton, L. V., Ndao, I. M., Tarr, P. I., Warner, B. B., & Gordon, J. I. (2016) · Nature · doi:10.1038/nature17940 · Cited by 320
Zachos, N. C., Kovbasnjuk, O. N., Foulke-Abel, J. D., In, J., Blutt, S. E., de Jonge, H. R., Estes, M. K., & Donowitz, M. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.r114.635995 · Cited by 308
Gustafsson, J. K., Ermund, A., Johansson, M., Schutte, A. H., Hansson, G. C., & Sjövall, H. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00405.2011 · Cited by 251
The microenvironment of injured murine gut elicits a local pro-restitutive microbiota
Alam, A. M., Leoni, G., Quirós, M., Wu, H., Desai, C., Nishio, H., Jones, R. M., Nusrat, A., & Neish, A. S. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2015.21 · Cited by 243
Human secretory immunoglobulin A may contribute to biofilm formation in the gut
Bollinger, R. R., Everett, M. L., Palestrant, D., Love, S. D., Lin, S. S., & Parker, W. (2003) · Immunology · doi:10.1046/j.1365-2567.2003.01700.x · Cited by 209
Microbial Colonization of the Upper Gastrointestinal Tract in Patients with Barrett's Esophagus
Macfarlane, S., Furrie, E., Macfarlane, G. T., & Dillon, J. F. (2007) · Clinical Infectious Diseases · doi:10.1086/518578 · Cited by 184
Licht, T. R., Christensen, B. B., Krogfelt, K. A., & Molin, S. (1999) · Microbiology · doi:10.1099/00221287-145-9-2615 · Cited by 167
The microbiome in wound repair and tissue fibrosis
Scales, B. S., & Huffnagle, G. B. (2012) · The Journal of Pathology · doi:10.1002/path.4118 · Cited by 166
Microbial biofilms and the human intestinal microbiome
de Vos, W. M. (2015) · npj Biofilms and Microbiomes · doi:10.1038/npjbiofilms.2015.5 · Cited by 163
Biofilm-growing intestinal anaerobic bacteria
Donelli, G., Vuotto, C., Cardines, R., & Mastrantonio, P. (2012) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2012.00962.x · Cited by 148
Mucins Suppress Virulence Traits of Candida albicans
Kavanaugh, N. L., Zhang, A. Q., Nobile, C. J., Johnson, A. D., & Ribbeck, K. (2014) · mBio · doi:10.1128/mbio.01911-14 · Cited by 143
The immunological functions of the Appendix: An example of redundancy?
Girard-Madoux, M. J. H., de Agüero, M. G., Ganal-Vonarburg, S. C., Mooser, C., Belz, G. T., Macpherson, A. J., & Vivier, É. (2018) · Seminars in Immunology · doi:10.1016/j.smim.2018.02.005 · Cited by 131
Microbial Biofilms in the Gut: Visualization by Electron Microscopy and by Acridine Orange Staining
Palestrant, D., Holzknecht, Z. E., Collins, B. H., Parker, W., Miller, S., & Bollinger, R. R. (2004) · Ultrastructural Pathology · doi:10.1080/01913120490275196 · Cited by 129
Mucin Biopolymers Prevent Bacterial Aggregation by Retaining Cells in the Free-Swimming State
Caldara, M., Friedlander, R. S., Kavanaugh, N. L., Aizenberg, J., Foster, K. R., & Ribbeck, K. (2012) · Current Biology · doi:10.1016/j.cub.2012.10.028 · Cited by 127
Polymicrobial wound infections: Pathophysiology and current therapeutic approaches
Bertesteanu, S. V., Triaridis, S., Stankovic, M. D., Lazăr, V., Chifiriuc, M. C., Vlad, M., & Grigore, R. (2013) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2013.12.012 · Cited by 117
Mucosal Biofilm Communities in the Human Intestinal Tract
Macfarlane, S., Bahrami, B., & Macfarlane, G. T. (2011) · Advances in applied microbiology · doi:10.1016/b978-0-12-387046-9.00005-0 · Cited by 113
Bollinger, R. R., Everett, M. L., Wahl, S. D., Lee, Y.-H., Orndorff, P. E., & Parker, W. (2005) · Molecular Immunology · doi:10.1016/j.molimm.2005.02.013 · Cited by 112
Physical stress and bacterial colonization
Otto, M. J. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12088 · Cited by 100
Consequences of Biofilm and Sessile Growth in the Large Intestine
Macfarlane, S., McBain, A. J., & Macfarlane, G. T. (1997) · Advances in Dental Research · doi:10.1177/08959374970110011801 · Cited by 96
Bacterial biofilm within diseased pancreatic and biliary tracts
Swidsinski, A. V., Schlien, P., Pernthaler, A., Gottschalk, U., Bärlehner, E., Decker, G., Swidsinski, S., Strassburg, J., Loening-Baucke, V., Hoffmann, U., et al. (2005) · Gut · doi:10.1136/gut.2004.043059 · Cited by 89
Microbial Biofilms in the Gut: Visualization by Electron Microscopy and by Acridine Orange Staining
Palestrant, D., Holzknecht, Z. E., Collins, B. H., et al. (2004) · Ultrastructural Pathology · doi:10.1080/usp.28.1.23.27 · Cited by 70
Intestinal microbial flora after feeding phytohemagglutinin lectins (Phaseolus vulgaris) to rats
Banwell, J. G., Howard, R., Cooper, D., & Costerton, J. W. (1985) · Applied and Environmental Microbiology · doi:10.1128/aem.50.1.68-80.1985 · Cited by 69
Wake, N., Asahi, Y., Noiri, Y., Hayashi, M., Motooka, D., Nakamura, S., Gotoh, K., Miura, J., Machi, H., Iida, T., et al. (2016) · npj Biofilms and Microbiomes · doi:10.1038/npjbiofilms.2016.18 · Cited by 69
Biofilm andHelicobacter pylori: From environment to human host
García, A. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i19.5632 · Cited by 68
Treatment of an atazanivir associated grade 4 hyperbilirubinaemia with efavirenz: Figure 1
Kummer, O., Mossdorf, E., Battegay, M., Elzi, L., Bodmer, M., Krähenbühl, S., & Haschke, M. (2007) · Gut · doi:10.1136/gut.2007.126144 · Cited by 63
Immune exclusion and immune inclusion: a new model of host-bacterial interactions in the gut
Everett, M. L., Palestrant, D., Miller, S., Bollinger, R. R., & Parker, W. (2004) · Clinical and Applied Immunology Reviews · doi:10.1016/j.cair.2004.03.001 · Cited by 59
McDonald, J. A. K., Fuentes, S., Schroeter, K., Jong, I. H., Khursigara, C. M., de Vos, W. M., & Allen‐Vercoe, E. (2014) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2014.11.007 · Cited by 59
Dishaw, L. J., Leigh, B. A., Cannon, J. P., Liberti, A., Mueller, M. G., Skapura, D. P., Karrer, C. R., Pinto, M. R., Santis, R. D., & Litman, G. W. (2016) · Nature Communications · doi:10.1038/ncomms10617 · Cited by 57
Sugar Coating the Envelope: Glycoconjugates for Microbe–Host Crosstalk
Tytgat, H. L. P., & de Vos, W. M. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.06.004 · Cited by 57
Self-citationMorphological evolution of the mammalian cecum and cecal appendix
Smith, H. F., Parker, W., Kotzé, S. H., & Laurin, M. (2017) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2016.06.001 · Cited by 51
Research works printed but not linked: 1
- Bollinger, 2007, Biofilms in the normal human large bowel: fact rather than fiction, Gut, 56, 1481
Cited by
Sorted by citations
Fassarella, M., Blaak, E. E., Penders, J., Nauta, A., Smidt, H., & Zoetendal, E. G. (2020) · Gut · doi:10.1136/gutjnl-2020-321747 · Cited by 818
The gut microbiota and its biogeography
McCallum, G., & Tropini, C. (2023) · Nature Reviews Microbiology · doi:10.1038/s41579-023-00969-0 · Cited by 361
Gastrointestinal biofilms in health and disease
Motta, J., Wallace, J. L., Buret, A. G., Deraison, C., & Vergnolle, N. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-00397-y · Cited by 291
Biofilm Resilience: Molecular Mechanisms Driving Antibiotic Resistance in Clinical Contexts
Almatroudi, A. (2025) · Biology · doi:10.3390/biology14020165 · Cited by 230
Escherichia coli Residency in the Gut of Healthy Human Adults
Martinson, J. N. V., & Walk, S. T. (2020) · EcoSal Plus · doi:10.1128/ecosalplus.esp-0003-2020 · Cited by 197
Metadata
- Authors
- Tytgat, H. L. P., Nobrega, F. L., van der Oost, J., & de Vos, W. M.
- Affiliations
- ETH Zurich (CH)
- Corresponding author
- Tytgat, Hanne L.P.
- ORCID
- Tytgat, Hanne L.P.
- Venue
- Trends in Microbiology
- Publisher
- Elsevier BV
- Published
- 2019-01
- Volume
- 27
- Issue
- 1
- Pages
- 17-25
- ISSN
- 0966-842X (ISSN-L)
- OpenAlex
- W2890494833
- Cited by
- 144
- References
- 62
- Citations by year
- 2026: 6 · 2025: 20 · 2024: 22 · 2023: 27 · 2022: 19 · 2021: 24 · 2020: 15 · 2019: 10
- FWCI
- 1.23
- Type
- journal article
- Language
- en
- Open access
- green
- research.wur.nl
- Locations
- Trends in Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- Repository for Publications and Research Data (ETH Zurich) (acceptedVersion, cc-by-nc-nd)
- ePrints Soton (University of Southampton) (submittedVersion)
- Työväentutkimus Vuosikirja (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- ETH Zürich Research Collection
- Funders
- ERC grant Microbes Inside (250172)
- Soehngen Institute of Anaerobic Microbiology (024.002.002)
- The Netherlands Organization for Scientific Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Keywords
- polymicrobial biofilms, gut microbiota, intestinal mucosa, biomarkers, microcolonies, intestinal diseases, colon cancer
- MeSH terms
- Gastrointestinal Microbiome, Bacteria, Bacterial Infections, Colon, Humans, Biomarkers, Biofilms, Microbiota
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
