The DOI matches its Crossref record; 231 of the 232 references it cites were found in a registry or an index.
Can probiotics modulate human disease by impacting intestinal barrier function?
Open accessAbstract
Intestinal barrier integrity is a prerequisite for homeostasis of mucosal function, which is balanced to maximise absorptive capacity, while maintaining efficient defensive reactions against chemical and microbial challenges. Evidence is mounting that disruption of epithelial barrier integrity is one of the major aetiological factors associated with several gastrointestinal diseases, including infection by pathogens, obesity and diabetes, necrotising enterocolitis, irritable bowel syndrome and inflammatory bowel disease. The notion that specific probiotic bacterial strains can affect barrier integrity fuelled research in which in vitro cell lines, animal models and clinical trials are used to assess whether probiotics can revert the diseased state back to homeostasis and health. This review catalogues and categorises the lines of evidence available in literature for the role of probiotics in epithelial integrity and, consequently, their beneficial effect for the reduction of gastrointestinal disease symptoms.
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In the citing paper
“There is substantial evidence that probiotics can strengthen the intestinal barrier, regulate mucosal immune function, and produce metabolites beneficial to the host to maintain health, as illustrated in Figure 1 [22,23].”
From Probiotics Regulate Gut Microbiota: An Effective Method to Improve Immunity (2021) · cites this paper as [22]
In the citing paper
“a variety of studies do suggest that probiotics are able to improve mucosal barrier function (Bron et al., 2017).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Bron et al., 2017
In the citing paper
“There is compelling evidence that probiotics are able to support the intestinal barrier (Bron et al., 2017), which may act to dampen the increased inflammatory tone seen in aging and enhance the immune response to viral infections and vaccinations.”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Bron et al., 2017
In the citing paper
“The GI microbiome is thought to be a key player in this process as it is essential for the proper maintenance of the intestinal barrier through various mechanisms, e.g., production of SCFA (Bron et al., 2017) as well as tryptophan metabolites (Rothhammer and Quintana, 2019).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Bron et al., 2017
In the citing paper
“Similar as the endogenous microbiota, probiotics may improve mucosal barrier function, limiting the ability of viral particles to cross this physical barrier and maintain this barrier during viral disease (Bron et al., 2017).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Bron et al., 2017
In the citing paper
“Numerous pre-clinical studies have shown that oral probiotics are capable of positively influencing gut barrier function and systemic immunity, and thus, in the case of pneumonia, may enhance the host’s ability to suppress and clear reproducing lung pathogens as they emerge (Bron et al., 2017) (Forsythe, 2014).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Bron et al., 2017
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Citations
Cites
1 retracted
Items 201–231 of 231
Sever Sepsis After Probiotic Treatment With Escherichia coli NISSLE 1917
Guenther, K., Straube, E., Pfister, W., Guenther, A., & Huebler, A. (2010) · Pediatric Infectious Disease Journal · doi:10.1097/inf.0b013e3181c36eb9 · Cited by 63 · cited 1×
“infants and, although cases of sepsis due to probiotic administration have been occasionally described in preterm((167)) and immunocompromised patients((168)), these cases remain rare.”
BackgroundSovran, B., Loonen, L. M. P., Lü, P., Hugenholtz, F., Belzer, C., Stolte, E. H., Boekschoten, M. V., van Baarlen, P., Kleerebezem, M., de Vos, P., et al. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000319 · Cited by 62 · cited 1×
“Moreover, in mucus-deficient mice, the ileal region of the intestine appears to be protected from excessive inflammatory responses by activation of epithelial repair and barrier maintenance pathways through the IL-22-STAT regulatory axis((12)).”
BackgroundProbiotics in the Prevention of Necrotizing Enterocolitis
Ganguli, K. A., & Walker, W. A. (2011) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e318228b799 · Cited by 60
Emara, M., Elhawari, S. A., Yousef, S., Radwan, M. I., & Abdel‐Aziz, H. R. (2015) · Helicobacter · doi:10.1111/hel.12237 · Cited by 57
Influence and effect of the human microbiome in allergy and asthma
Panzer, A. R., & Lynch, S. V. (2015) · Current Opinion in Rheumatology · doi:10.1097/bor.0000000000000191 · Cited by 55 · cited 1×
“In addition, several other diseases also appear to be associated with a ‘leaky’ gut phenotype, including the post-infectious subtype of IBS((224)), and possibly also allergy((225)).”
BackgroundHabil, N., Abate, W., Beal, J., & Foey, A. (2014) · Beneficial Microbes · doi:10.3920/bm2013.0061 · Cited by 55
Microecology, intestinal epithelial barrier and necrotizing enterocolitis
Sharma, R. R., & Tepas, J. J. (2009) · Pediatric Surgery International · doi:10.1007/s00383-009-2536-2 · Cited by 52
Cilieborg, M. S., Thymann, T., Siggers, R. H., Boyé, M., Bering, S. B., Jensen, B. B., & Sangild, P. T. (2010) · Journal of Nutrition · doi:10.3945/jn.110.128561 · Cited by 52 · cited 2×
“As discussed by the authors, the results in the piglet study may be explained by experimental bias and would require confirmation((166)).”
BackgroundResultChrzanowska-Liszewska, D., Seliga-Siwecka, J. P., & Borszewska-Kornacka, M. K. (2011) · Early Human Development · doi:10.1016/j.earlhumdev.2011.07.002 · Cited by 51
Host-Recognition of Pathogens and Commensals in the Mammalian Intestine
Rossi, O., van Baarlen, P., & Wells, J. M. (2011) · Current topics in microbiology and immunology · doi:10.1007/82_2011_191 · Cited by 50 · cited 8×
“Mucosal Ig and antimicrobial peptides (AMP) and proteins secreted by the epithelial cells serve to enhance the barrier function of the epithelium through immune exclusion and killing of bacteria((11)).”
BackgroundInfluentialZhang, W., GU, Y.-R., Chen, Y., Deng, H. X., Chen, L., Chen, S., Zhang, G., & Gao, Z. (2010) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0b013e32833eb8b0 · Cited by 50
Bermúdez-Brito, M., Muñoz‐Quezada, S., Gómez‐Llorente, C., Matencio, E., Romero, F., & Gil, Á. (2015) · BMC Microbiology · doi:10.1186/s12866-015-0408-6 · Cited by 48
Underwood, M. A., Kananurak, A., Coursodon, C. F., Adkins-Reick, C. K., Chu, H., Bennett, S. H., Wehkamp, J., Castillo, P. A., Leonard, B. C., Tancredi, D. J., et al. (2012) · Pediatric Research · doi:10.1038/pr.2012.11 · Cited by 47 · cited 1×
“Moreover, in these models, the mucosal expression of various factors involved in barrier function regulation and maintenance could be normalised by probiotic supplementation, including TLR4((158)) and TLR9((159)), mucin and trefoil factor (TFF)((160)) and antimicrobial protein and peptides((161)).”
BackgroundAsahara, T., Shimizu, K., Takada, T., KADO, S., Yuki, N., Morotomi, M., Tanaka, R., & Nomoto, K. (2010) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2010.04884.x · Cited by 47
König, J., & Brummer, R. J. (2014) · Beneficial Microbes · doi:10.3920/bm2013.0033 · Cited by 43 · cited 1×
“Overall, the results of these trials are difficult to interpret, because of the use of different strains and combinations thereof, as well as limitations in the study designs((186)).”
BackgroundRossi, O., Karczewski, J., Stolte, E. H., Brummer, R. J., van Nieuwenhoven, M. A., Meijerink, M., van Neerven, R. J. J., van IJzendoorn, S. C. D., van Baarlen, P., & Wells, J. M. (2013) · BMC Research Notes · doi:10.1186/1756-0500-6-431 · Cited by 43
ten Bruggencate, S. J. M., Girard, S., Vollenbroek, E. G. M., Bhardwaj, R., & Tompkins, T. A. (2014) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2014.238 · Cited by 35 · cited 1×
“Nevertheless, these models have been used to study the protective capacity of probiotics and other dietary ingredient interventions, with generally poor success rates for probiotics in the amelioration of diarrhoea symptoms((30,31)).”
MethodThe design of probiotic studies to substantiate health claims.
Gibson, G. R., Brummer, R. J., Isolauri, E., Lochs, H. H., Morelli, L., Ockhuizen, T., Rowland, I. R., Schrezenmeir, J., Stanton, C., & Verbeke, K. (2011) · Gut Microbes · doi:10.4161/gmic.2.5.18002 · Cited by 35
Intestinal Barrier Function and Cow's Milk Sensitization in Guinea Pigs Fed Milk or Fermented Milk
Terpend, K., Blaton, M. A., Candalh, C., Wal, J., Pochart, P., & Heyman, M. (1999) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-199902000-00019 · Cited by 34
Ouwehand, A. C., ten Bruggencate, S. J. M., Schonewille, A. J., Alhoniemi, E. J., Forssten, S. D., & Bovee-Oudenhoven, I. M. J. (2013) · British Journal Of Nutrition · doi:10.1017/s0007114513002547 · Cited by 29 · cited 1×
“Nevertheless, these models have been used to study the protective capacity of probiotics and other dietary ingredient interventions, with generally poor success rates for probiotics in the amelioration of diarrhoea symptoms((30,31)).”
MethodMcVay, M. R., Boneti, C., Habib, C. M., Keller, J. E., Kokoska, E. R., Jackson, R. J., & Smith, S. D. (2008) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2007.09.013 · Cited by 29
Manzoni, P. (2007) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/01.mpg.0000302971.06115.15 · Cited by 28
Omics approaches to study host–microbiota interactions
van Baarlen, P., Kleerebezem, M., & Wells, J. M. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.07.001 · Cited by 27 · cited 1×
“The human intestine contains a dense and complex community of microbes, and many representatives permanently inhabit this niche((1,2)).”
BackgroundGonçalves, F. L. L., Soares, L. M. M., Figueira, R. L., Simões, A. L. B., Gallindo, R. M., & Sbragia, L. (2014) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2014.07.007 · Cited by 25
Bujalance, C., Jiménez‐Valera, M., Moreno, E., Ruiz‐López, M. D., Lasserrot, A., & Ruiz‐Bravo, A. (2013) · Research in Microbiology · doi:10.1016/j.resmic.2013.10.006 · Cited by 24 · cited 2×
“In this area, various rodent in vivo((35)) infection models have demonstrated that probiotics can attenuate the severity of infection caused by several gastrointestinal pathogens, including H.”
BackgroundMihatsch, W. (2011) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e3283454e78 · Cited by 24 · cited 1×
“small trials that use different probiotic strains((126,127)).”
Fåk, F., Ahrné, S., Linderoth, A., Molin, G., Jeppsson, B. W., & Weström, B. R. (2007) · Digestive Diseases and Sciences · doi:10.1007/s10620-007-9906-1 · Cited by 19
Novel opportunities for the exploitation of host–microbiome interactions in the intestine
Claes, I. J. J., Garcia, C. V., & Lebeer, S. (2014) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2014.10.008 · Cited by 16 · cited 1×
“The human intestine contains a dense and complex community of microbes, and many representatives permanently inhabit this niche((1,2)).”
BackgroundMultispecies probiotic protects gut barrier function in experimental models
Mylene, Nébot-Vivinus, Cherryl, Harkat, Hanene, Bzioueche, Christel, Cartier, Raffaella, Plichon-Dainese, et al. (2014) · Acta Scientiarum Naturalium Universitatis Sunyatseni · Cited by 16
[Irritable Bowel Syndrome; gut microbiota and probiotic therapy].
González, R. T., Gonzalez, A. S., Madiedo, P. R., Mata, A. M., Muniz, M. P., Alonso, E. B., Llorente, F. J. R., Villar, M. C. M., González, M. M. A., Diaz, M. F. V., et al. (2015) · PubMed · doi:10.3305/nh.2015.31.sup1.8713 · Cited by 6
Wang, G., Feng, Y., Wang, Y., Huang, N., Wu, Q., & Wang, B. (2003) · PubMed · Cited by 6
Research works printed but not linked: 1
- 10.1172/JCI20514 · DOI · Paper page
Cited by
Sorted by citations
Mucus barrier, mucins and gut microbiota: the expected slimy partners?
Paone, P., & Cani, P. D. (2020) · Gut · doi:10.1136/gutjnl-2020-322260 · Cited by 1,665
Human gut microbiota/microbiome in health and diseases: a review
Gomaa, E. Z. (2020) · Antonie van Leeuwenhoek · doi:10.1007/s10482-020-01474-7 · Cited by 1,294
Regulation of the intestinal barrier by nutrients: The role of tight junctions
Suzuki, T. (2020) · Animal Science Journal · doi:10.1111/asj.13357 · Cited by 796
“These aspects are not extensively discussed in the current review as they have been recently reviewed elsewhere (Bron et al., 2017; Hiippala et al., 2018).”
BackgroundFermented foods in a global age: east meets West
Tamang, J. P., Cotter, P. D., Endo, A., Han, N. S., Kort, R., Liu, S. Q., Mayo, B., Westerik, N., & Hutkins, R. (2020) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12520 · Cited by 719
Li, P., Wang, H., Guo, L., Gou, X., Chen, G., Lin, D., Fan, D., Guo, X., & Liu, Z. (2022) · BMC Medicine · doi:10.1186/s12916-022-02657-x · Cited by 581
“Although the present study did not find a causal effect of bacteria, which were previously reported to impair the intestinal barrier in PE, some probiotics such as Bifidobacterium have been reported to stimulate the expression of Mucins 3 in intestinal epithelial cells [67] and restore mucus growth [68], thereby maint…”
Result
Metadata
- Authors
- Bron, P. A., Kleerebezem, M., Brummer, R.-J., Cani, P. D., Mercenier, A., MacDonald, T. T., Garcia-Ródenas, C. L., & Wells, J. M.
- Affiliations
- Nederlands Instituut Voor Zuivel Oonderzoek (NL)
- Wageningen University & Research (NL)
- Örebro University (SE)
- Walloon Excellence in Lifesciences and Biotechnology (BE)
- Nestlé (Switzerland) (CH)
- Queen Mary University of London (GB)
- Corresponding author
- Bron, Peter A.
- ORCID
- Venue
- British Journal Of Nutrition
- Publisher
- Cambridge University Press (CUP)
- Published
- 2017-01-14
- Volume
- 117
- Issue
- 1
- Pages
- 93-107
- ISSN
- 0007-1145 (ISSN-L)
- 1475-2662
- PMC
- PMC5297585
- OpenAlex
- W2573938105
- Cited by
- 499
- References
- 232
- Citations by year
- 2026: 54 · 2025: 47 · 2024: 55 · 2023: 52 · 2022: 64 · 2021: 67 · 2020: 54 · 2019: 43 · 2018: 42 · 2017: 19
- FWCI
- 4.68
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- British Journal Of Nutrition (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion, cc-by-nc-nd)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion, other-oa)
- Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by-nc-nd)
- Data Archiving and Networked Services (DANS) (submittedVersion, cc-by-nc-nd)
- Funders
- Fonds De La Recherche Scientifique - FNRS (WELBIO-CR-2012S-02R)
- Walloon excellence in life sciences and biotechnology
- FP7 Ideas: European Research Council (336452)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- probiotics, intestinal barrier function, epithelial barrier integrity, mucosal homeostasis, gastrointestinal diseases, irritable bowel syndrome, inflammatory bowel disease, necrotizing enterocolitis, obesity, diabetes mellitus, pathogen infection
- MeSH terms
- Animals, Humans, Intestinal Diseases, Intestines, Probiotics
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