The DOI matches its Crossref record; 55 of the 55 references it cites were found in a registry or an index.
Microbial biofilms in the human gastrointestinal tract
Abstract
The human gastrointestinal tract contains rich and diverse microbiotas along its length. However, while extensive studies have been made on lumenal bacterial communities in the gut, less work has been carried out on organisms growing in biofilms, where individual groups of bacteria exist in a multiplicity of different microhabitats and metabolic niches associated with the mucosa, the mucus layer and particulate surfaces in the gut lumen. Bacteria and yeasts also occur in biofilms attached to artificial surfaces and devices implanted in the host, such as in patients being fed via enteral tubes. Although we are just beginning to investigate the composition and metabolic activities of these structures, increasing evidence suggests that they are important to the host in both health and disease. There is mounting interest in mucosal biofilms in the colon, especially with respect to their role in inflammatory bowel disease. Because bacteria growing in biofilms are more resistant to antibiotics than unattached organisms, it is often difficult to modify the structure and composition of these communities, or to eradicate them from the body. However, recent work has shown that there is considerable potential to alter the species composition of mucosal biofilms in a beneficial way using synbiotics.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
In the citing paper
“The size and quality of the intestinal mucus layer is believed to be mediated by sympathetic innervation where mucosal immune system modulation (Elenkov et al., 2000) and microbial composition and behavior alterations (commensal and pathogenic) were seen (Macfarlane and Dillon, 2007;Rhee et al., 2009)”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Macfarlane and Dillon, 2007
In the citing paper
“The ANS-mediated modulation of mucus secretion is likely to have important effects on the size and quality of the intestinal mucus layer, an important habitat for the biofilm, where the majority of the enteric microbiota reside.19”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [19]
In the citing paper
“In general, bacteria located in the biofilm seem to be less affected by environmental alterations, such as changes in intestinal transit rate and luminal contents, than luminal populations are, but seem to have increased involvement in bidirectional signaling with the host.19”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [19]
Citations
Cites
Suau, A., Bonnet, R., Sutren, M., Godon, J.-J., Gibson, G. R., Collins, M. D., & Doré, J. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.11.4799-4807.1999 · Cited by 1,490
Rembacken, B., Snelling, A. M., Hawkey, P. M., Chalmers, D. M., & Axon, A. (1999) · The Lancet · doi:10.1016/s0140-6736(98)06343-0 · Cited by 1,100
Influence of interfaces on microbial activity
van Loosdrecht, M. C. M., Lyklema, J., Norde, W., & Zehnder, A. J. B. (1990) · Microbiological Reviews · doi:10.1128/mr.54.1.75-87.1990 · Cited by 875
Zoetendal, E. G., von Wright, A., Vilpponen-Salmela, T., Ben-Amor, K., Akkermans, A. D. L., & de Vos, W. M. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.7.3401-3407.2002 · Cited by 868
Physiology of the Gastrointestinal Tract
Clayman, C. Β. (1981) · JAMA · doi:10.1001/jama.1981.03320240069035 · Cited by 814
Kruis, W., SCHÜTZ, E., Fric, P., Fixa, B., Judmaier, G., & Stolte, M. (1997) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.1997.00225.x · Cited by 774
Furrie, E., Macfarlane, S., Kennedy, A., Cummings, J. H., Walsh, S. V., O’Neil, D. A., & Macfarlane, G. T. (2005) · Gut · doi:10.1136/gut.2004.044834 · Cited by 766
Self-citationAdsorption of Microorganisms to Surfaces. 1980
Bitton, G., & Marshall, K. C. (1980) · Soil Science · doi:10.1097/00010694-198011000-00012 · Cited by 613
Lin, J.-S., Lee, I. S., Frey, J., Slonczewski, J. L., & Foster, J. W. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.14.4097-4104.1995 · Cited by 569
Venturi, Gionchetti, P., Rizzello, F., Johansson, Zucconi, Brigidi, P., Matteuzzi, & Campieri, M. (1999) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.1999.00560.x · Cited by 567
Research works printed but not linked: 7
- Cabre E., 1993, Nutrition, 9, 1
- Cohen M.B., 1991, The Large Intestine: Physiology, Pathophysiology and Disease, 395
- Cummings J.H., 2003, Curr Issues Intest Microbiol, 4, 9
- van Loosdrecht M.C.M., 1990, Microbiol Rev, 54, 75, 10.1128/MMBR.54.1.75-87.1990 · DOI
- Macfarlane G.T., 1991, The Colonic Flora, Fermentation and Large Bowel Digestive Function, 51
- Macfarlane G.T., 1995, Gastrointestinal and Oesophageal Physiology, 249
- Rembacken B.J., 1999, Lancet, 354, 636
Cited by
Sorted by citations
Items 301–374 of 374
Role of Microbiota-Derived Exosomes in Gut–Brain Communication for the Treatment of Brain Disorders
Agnihotri, T. G., Gomte, S. S., Peddinti, V., Rout, B., Shewale, R. S., Janjal, P., & Jain, A. (2024) · Springer eBooks · doi:10.1007/978-981-99-8373-5_9 · Cited by 1
INVESTIGATION OF ZONULIN LEVELS IN DOGS INFECTED WITH CANINE DISTEMPER VIRUS
Çöllü, E. M., Özalp, T., ERDOĞAN, S., Ural, K., & Erdoğan, H. (2024) · Bozok Veterinary Sciences · doi:10.58833/bozokvetsci.1545898 · Cited by 1
Rubio-Cervantes, I., Wolfrum, S., Wolfgang, S., Rodehutscord, M., & Camarinha‐Silva, A. (2025) · Poultry Science · doi:10.1016/j.psj.2025.106209 · Cited by 1
“This may reflect the role of Ca in promoting bacterial aggregation and altering spatial distribution within the gut (Macfarlane and Dillon, 2007).”
The brain–gut–joint axis in arthritis: crosstalk, treatment, and future perspectives
Zhong, S., Li, F., Li, D., Cheng, Y., Wang, X., Gao, Y., & Xie, X. (2026) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2025.101045 · Cited by 3
“Additionally, ANS may also impact the intestinal micro-environment by influencing the regulation of mucus secretion, the activation of the intestinal immune system, and other mechanisms [104, 105].”
Microbial shifts in early life: the pediatric gut microbiome and its role in health and disease
Waghmode, S., Viswanathan, R., Koligudde, V., Umare, P., & Lavania, M. (2026) · Gut Microbes · doi:10.1080/19490976.2026.2681763 · Cited by 1
Coaggregation of Gut Bacteroides & Parabacteroides with Probiotic Lactobacillus Rhamnosus GG
Schotten, S. (2016) · Cited by 1
Peripheral and Central Mechanisms in Irritable Bowel Syndrome : in search of links
Bednarska, O. (2019) · Linköping University medical dissertations · doi:10.3384/diss.diva-156669 · Cited by 1
Biofilm formation by the anaerobic pathogen Clostridium difficile
Cellulare, B., Moleculare, E., Xxvi, C., Đapa, T., Scarlato, V., & Unnikrishnan, M. (2014) · Cited by 1
Shah, F., & Dwivedi, M. (2022) · Springer eBooks · doi:10.1007/978-981-16-6760-2_4 · Cited by 1
Mujezinovic, S. C. (2022) · Bacterial Empire · doi:10.36547/be.501 · Cited by 1
Davis, T. L., Dirks, B., Carnero, E. Á., Corbin, K. D., Smith, S. R., Marcus, A. K., Krajmalnik‐Brown, R., & Rittmann, B. E. (2026) · PLoS ONE · doi:10.1371/journal.pone.0347668 · Cited by 3
“Some evidence indicates that microorganisms in epithelial biofilms influence bowel inflammation and dysbiosis [57,58], while methanogens, specifically, M. smithii , have been linked to obesity [59] and anorexia [60].”
Gutiérrez-Escobar, A. J., Bayona, M. A., Barragan-Vidal, C., Lara, S. R., & Oliveros, R. (2014) · PubMed · doi:10.47892/rgp.2014.343.158 · Cited by 1
Cucurbit Extracts Augment Biofilm Formation by Probiotic Lactobacilli: An In Vitro Study
Irfan, A., Asad Khan, M., Syed Hassan, M., Zafaryab, M., Ahmad, P. I., & M, M. A. R. (2017) · Journal of Microbial & Biochemical Technology · doi:10.4172/1948-5948.1000354 · Cited by 1
“Gut-associated biofilm of probiotic bacterial communities modulate enteric barrier functions and immunity [17].”
BackgroundBACTERIOPHAGES AND THEIR EFFECT ON BACTERIAL BIOFILMS
Воробєй, Є. С., Voronkova, O. S., Маліновська, I. В., & Винников, А. И. (2013) · Microbiology&Biotechnology · doi:10.18524/2307-4663.2013.1(21).48707 · Cited by 1
Introduction of Microbial as a Major Factor in the Human Body
Hosseini, S. M. F., & Aiubi, S. (2019) · International Journal of Advanced Biological and Biomedical Research · doi:10.33945/sami/ijabbr.2020.2.3 · Cited by 1
The Role of Biofilm in Originating, Mediating, and Proliferating Infectious Diseases
Singh, A. K., Gaur, V., & Maurya, A. K. (2019) · Springer eBooks · doi:10.1007/978-3-030-30757-8_4 · Cited by 1
The importance of intestinal dysbiosis in mood disorders
Wójcik, M., Boreński, G., Poleszak, J., Szabat, M., Złakowska, P., & Milanowska, J. (2019) · World Scientific News · Cited by 1
The Use of Bioinformatic Tools in Symbiosis and Co-Evolution Studies
Valle-Gough, R. E., Samaniego-Gámez, B. Y., Apodaca-Hernández, J. E., & Arena-Ortíz, M. L. (2020) · Metagenomics · doi:10.5772/intechopen.86559 · Cited by 1
“mellifera, Litopenaeus vannamei, Mus musculus, Homo sapiens) have been reported as necessary for survival, since their cooperative behavior increases the vigor of a community [28, 39, 47, 49, 50].”
BackgroundInflammation, stress, and gut-brain axis as therapeutic targets in bipolar disorder
Vaccariello, E. D., & Nguyen, T. T. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-821398-8.00008-4 · Cited by 1
Microbiota, biofilms and Helicobacter pylori in the diseases of gastroduodenal zone
Isaeva, G. S., & Зиатдинов, В. Б. (2014) · Kazan medical journal · doi:10.17816/kmj2232 · Cited by 1
In vitroModels of Host–Microbial Interactions Within the Gastrointestinal Tract
Özcan, E., Levantovsky, R. M., & Sela, D. A. (2018) · Wiley eBooks · doi:10.1002/9781118823309.ch4 · Cited by 1
Sisk-Hackworth, L., Brown, J., Sau, L., Levine, A. A., Tam, L. Y. I., Ramesh, A., Shah, R. S., Kelley-Thackray, E. T., Wang, S., Nguyen, A., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.20.545808 · Cited by 1
Adaptation of Enterococcus faecalis to intestinal mucus revealed by a human colonic organoid modelPreprint
Mikhaleva, S., Hsiao, P.-L., Kurmashev, A., Anderson, C. M., Colomer‐Winter, C., Boos, J. A., Choo, P. Y., Willett, J. L. E., Hierlemann, A. R., Kline, K. A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.20.670035 · Cited by 1
Regulation of biofilm formation in Salmonella typhimurium and Escherichia coli Nissle 1917
Monteiro, C. (2010) · Figshare
Role of c-di-GMP signalling in bacterial-host interactions
Lamprokostopoulou, A. (2010) · Figshare
The role of Enterococcal Surface Protein in the pathogenesis of Enterococcus faecium infections
Heikens, E. (2009) · Utrecht University Repository (Utrecht University)
Jack, L. (2014) · Faculty of Health; Institute of Health and Biomedical Innovation; School of Nursing
Candee, A. (2014)
Inflammation, Microflora, Motility, and Visceral Sensitivity
Michail, S. K., & Ng, M.-W. (2012) · Humana Press eBooks · doi:10.1007/978-1-60761-709-9_5
Inter-Kingdom Signaling Interactions in Enterohemorrhagic Escherichia coli Infections
Bansal, T. (2010) · OakTrust (Texas A&M University Libraries)
Clinical Implications of Interkingdom Fungal and Bacterial Biofilms
Ramage, G., O’Donnell, L. E., Kean, R., Townsend, E. R., & Rajendran, R. (2017) · CRC Press eBooks · doi:10.4324/9781315120119-2 · Cited by 1
Host–Biofilm Interactions at Mucosal Surfaces and Implications in Human Health
Venkiteswaran, N., Ellepola, K., Seneviratne, C. J., Lee, Y. K., Puan, K. J., & Wong, S. C. (2017) · Routledge eBooks · doi:10.4324/9781315120119-9
Ismail, K. A., Rezk, H. M., AlOtabi, M. M., Elthabati, W. S., & Khalifa, A. M. (2018) · Trends in Medicine · doi:10.15761/tim.1000121
“Studies have shown that a pH of lower than 4 is effective in limiting the growth of bacteria [15].”
BackgroundExploring the evolutionary link between biofilms and spores formation in spore-formers
Portinha, I. C. (2015) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Transcriptomic changes of the gut in dairy calves during pre-weaned period
Liang, G. (2016) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r39882v9t
Ma’moun, S. A. M., & Farag, R. (2019) · Egyptian Academic Journal of Biological Sciences. D, Histology and Histochemistry · doi:10.21608/eajbsd.2019.43363
Biofilm-mediated Gastrointestinal Diseases
Nayak, S. K. (2019) · Springer eBooks · doi:10.1007/978-3-030-30757-8_12
Comorbidity of irritable bowel syndrome and obesity
Simanenkov, V. I., Викторович, Т. С., & Dekkanova, V. D. (2020) · Medical alphabet · doi:10.33667/2078-5631-2020-10-11-16
Structure and Role of P. aeruginosa AlgL in Alginate Biosynthesis
Wong, S. (2016) · TSpace (University of Toronto)
Diet, Microbioma, and Diabetes in Aging
Fernández, S. S. M., & Ribeiro, S. M. L. (2020) · Current Geriatrics Reports · doi:10.1007/s13670-020-00339-1
Intestinal Mucosal Characteristic Flora in Diarrhea with Intestinal Dampness-Heat SyndromePreprint
Li, X., Long, C., & Tan, Z. (2021) · Research Square · doi:10.21203/rs.3.rs-612204/v1
Micronutrient intervention effects on cognitive outcomes in post-acute traumatic brain injury
Denniss, R. J. (2020) · Sheffield Hallam University · doi:10.7190/shu-thesis-00356
The Molecular Mechanism of Alginate O-Acetylation in Pseudomonas aeruginosa
Ricer, T. (2014) · TSpace (University of Toronto)
Yang, N. (2011) · HAL · doi:10.70675/5015b6cbz75a2z4aa0z814az4ed75ef79fde
“…and confers better adaptation to and protection from harsh environment (Stewart & Costerton, 2001; Stewart, 2001; Engelberg-Kulka et al., 2005; Macfarlane & Dillon, 2007; Landini, 2009). te l-0 06 57 24 7, v er si on 1 - 6 Ja n 20 12 te l-0 06 57 24 7, v er si on 1 - 6 Ja n 20 12 2 1.1.1…”
InfluentialBeneficial microbes from human and animal intestines
Fernández-Ciganda, S., Fraga, M., & Zunino, P. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85170-1.00008-7
Bogyo, M. S., & Shen, A. (2011) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.10435957.11267056
Gut–brain communication: a novel application of probiotics
Das, S., Undhad, T. J., & Hati, S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-822238-6.00017-0
Impact of the gut microbiome on human health and diseases
Banik, S. P., Sehgal, S., Ghosh, R. B., & Das, A. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-822238-6.00026-1 · Cited by 1
Development of a four species biofilm to mimic the upper gut microbial communityPreprint
Marques, C. N. H., Tanzman, J. V., García‐Rodríguez, A., Kim, A., Tako, E., & Mahler, G. J. (2023) · Research Square · doi:10.21203/rs.3.rs-2782969/v1
Based on Uida-Yici-Lacz Primer for Evaluation of Fecal Coliform in Mine WaterPreprint
Qin, J., Ruiqi, W., Mengfei, Z., Jinbo, Z., Qin, J., & Xi, J. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4509177
Based on uidA-yicI-lacZ primer for evaluation of fecal coliform in mine water
Qin, J., Wang, R., Zhang, M., Zhao, J., Li, Y., & Xi, J. (2023) · Bioresource Technology Reports · doi:10.1016/j.biteb.2023.101661
Single-species and multispecies biofilms causing infections
Keller, L. E. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-19252-4.00002-x
Aminian-Dehkordi, J., Dickson, A. M., Valiei, A., & Mofrad, M. R. K. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.11.628036
Shlar, I., Gurianov, Y., & Poverenov, E. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5169991
Wang, S., Kou, G.-J., Zhao, X.-H., Huang, G., Wang, J., Tian, L., Zuo, X.-L., Li, Y.-Q., Wang, J., & Yu, Y.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26713619
Wang, S., Kou, G.-J., Zhao, X.-H., Huang, G., Wang, J., Tian, L., Zuo, X.-L., Li, Y.-Q., Wang, J., & Yu, Y.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26713613
Wang, S., Kou, G.-J., Zhao, X.-H., Huang, G., Wang, J., Tian, L., Zuo, X.-L., Li, Y.-Q., Wang, J., & Yu, Y.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26713616
Kim, J. E., Kwon, K. C., Jin, Y. J., Seol, A., Song, H. J., Roh, Y. J., Kim, T. R., Park, E. S., Park, G. H., Park, J. W., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24571762
Wang, S., Kou, G.-J., Zhao, X.-H., Huang, G., Wang, J., Tian, L., Zuo, X.-L., Yanqing, L. I., Wang, J., & Yu, Y.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26713622
Vizuete, M. D. P. S. (2014) · theses.fr (ABES) · doi:10.70675/04549528z27e1z425bz9398z0023e7d1fdd8
Formation and functions of biofilms in the gut anaerobe Bacteroides thetaiotaomicron
Mihajlovic, J. (2017) · theses.fr (ABES) · doi:10.70675/ccb19c47zb427z4507zbbfazd7fd1e12c71d
The ‘gut feeling’: Connecting neurodegenerative diseases and gut microbiota
Niyogi, S., & Basu, S. (2026) · The Microbe · doi:10.1016/j.microb.2026.100719
The role of the gut-brain axis and polyphenolic compounds in glioblastoma
Agnihotram, B., Mutiu, I. N., Chiou, H., McGowen, K., & Mazewski, C. (2026) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2026.110484
Muhring-Salamone, S., Herbeck, L. N., Kopecz, R., & Rosenhahn, A. (2026) · ACS Applied Bio Materials · doi:10.1021/acsabm.6c00895
Metadata
- Authors
- Macfarlane, S., & Dillon, J. F.
- Affiliations
- University of Dundee (GB)
- Corresponding author
- Macfarlane, S.
- Venue
- Journal of Applied Microbiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-05
- Volume
- 102
- Issue
- 5
- Pages
- 1187-1196
- ISSN
- 1364-5072 (ISSN-L)
- 1365-2672
- OpenAlex
- W2041418306
- Cited by
- 379
- References
- 55
- Citations by year
- 2026: 11 · 2025: 10 · 2024: 20 · 2023: 26 · 2022: 24 · 2021: 25 · 2020: 28 · 2019: 31 · 2018: 22 · 2017: 26 · 2016: 14 · 2015: 17 · 2014: 32 · 2013: 16 · 2012: 20
- FWCI
- 0.98
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (submittedVersion)
- 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
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- biofilm, gastrointestinal tract, gut microbiota, mucus layer, inflammatory bowel disease, antibiotic resistance, synbiotics
- MeSH terms
- Bacteria, Humans, Intestinal Mucosa, Biofilms, Probiotics, Gastrointestinal Tract
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
