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Increased rectal mucosal expression of interleukin 1beta in recently acquired post-infectious irritable bowel syndrome
Open accessAbstract
BACKGROUND AND AIMS: Chronic bowel disturbances resembling irritable bowel syndrome (IBS) develop in approximately 25% of patients after an episode of infectious diarrhoea. Although we have previously shown that psychosocial factors operating at the time of, or prior to, the acute illness appear to predict the development of post-infectious IBS (PI-IBS), our finding of an increased inflammatory cell number in the rectum persisting for at least three months after the acute infection suggested that there is also an organic component involved in the development of PI-IBS. To evaluate this further, we measured expressions of interleukin 1beta (IL-1beta) and its receptor antagonist (IL-1ra) in these patients to provide additional evidence that the pathogenesis of PI-IBS is underpinned by an inflammatory process. METHODS: Sequential rectal biopsy samples were prospectively obtained during and three months after acute gastroenteritis, from eight patients who developed post-infectious IBS (INF-IBS) and seven patients who returned to normal bowel habits after acute gastroenteritis (infection controls, INF-CON). Eighteen healthy volunteers who had not suffered from gastroenteritis in the preceding two years served as normal controls (NOR-CON). IL-1beta and IL-1ra gene expressions were assayed by reverse transcriptase-polymerase chain reaction, and their levels of expression were quantitated by optical densitometry after electrophoresis on agarose gel. RESULTS: INF-IBS patients exhibited significantly greater expression of IL-1beta mRNA in rectal biopsies than INF-CON patients both during and three months after acute gastroenteritis. Moreover, IL-1beta mRNA expression had increased in biopsies taken from INF-IBS patients at three months after the acute infection but no consistent change was observed in INF-CON patients. IL-1beta mRNA expression of INF-IBS patients at three months post gastroenteritis was significantly greater than NOR-CON whereas that of INF-CON patients was not significantly different from NOR-CON. Despite these differential changes in IL-1beta mRNA expression, no significant changes were observed in IL-1ra mRNA expression among the three groups. CONCLUSIONS: These findings indicate that those patients who develop IBS post infection exhibit greater IL-1beta mRNA expression, both during and after the infection, compared with individuals who do not develop PI-IBS. We conclude that such patients may be susceptible to inflammatory stimuli, and that inflammation may play a role in the pathogenesis of PI-IBS.
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In the citing paper
“Studies on mast cells and cytokines point out that inflammation is present in IBS. 2, 13-20”
From Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota (2008) · cites this paper as [16]
In the citing paper
“Evidence supporting this hypothesis includes increased concentrations of inflammatory/immune cells in intestinal tissue from IBS patients, altered levels of pro- and anti-inflammatory cytokines in the GI tract and peripheral blood of patients with IBS (Table 1) (11, 13, 24, 36, 46, 50, 51, 62, 73, 75, 89, 90, 94, 98, 102, 118, 121–124, 168, 174, 185, 187), and IBS-associated polymorphisms in genes”
From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [75]
In the citing paper
“Evidence supporting this hypothesis includes increased concentrations of inflammatory/immune cells in intestinal tissue from IBS patients, altered levels of pro- and anti-inflammatory cytokines in the GI tract and peripheral blood of patients with IBS (Table 1) (11, 13, 24, 36, 46, 50, 51, 62, 73, 75, 89, 90, 94, 98, 102, 118, 121–124, 168, 174, 185, 187), and IBS-associated polymorphisms in genes”
From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [75]
In the citing paper
“Levels of interleukin (IL)-1β mRNA may be increased in the small intestine, colon, and rectum of patients with PI-IBS compared with healthy controls (75, 187), supporting the hypothesis that low-grade inflammation is present in patients with PI-IBS.”
From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [75]
In the citing paper
“The importance of the interaction between the intestinal microbiota and immune system in IBS patients is demonstrated by a few studies in patients with PI-IBS, indicating activation of the GI immune system following the acute GI infection (57, 58, 75, 89, 94, 124, 168, 170, 187)”
From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [75]
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The functional gastrointestinal disorders and the Rome III process
Drossman, D. A. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.03.008 · Cited by 2,416
O’Mahony, L., McCarthy, J., Kelly, P., Hurley, G., Luo, F., Chen, K., O’Sullivan, G. C., Kiely, B., Collins, J. K., Shanahan, F., et al. (2005) · Gastroenterology · doi:10.1053/j.gastro.2004.11.050 · Cited by 1,448
Enck, P., Aziz, Q., Barbara, G., Farmer, A. D., Fukudo, S., Mayer, E. A., Niesler, B., Quigley, E. M. M., Rajilić-Stojanović, M. D., Schemann, M., et al. (2016) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2016.14 · Cited by 1,102
Postinfectious Irritable Bowel Syndrome
Spiller, R., & Garsed, K. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.02.074 · Cited by 1,024
Brain-gut-microbe communication in health and disease
Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00094 · Cited by 952
Metadata
- Authors
- Gwee, K.-A.
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2003-04-01
- Volume
- 52
- Issue
- 4
- Pages
- 523-526
- ISSN
- 0017-5749 (ISSN-L)
- PMC
- PMC1773606
- OpenAlex
- W2148823535
- Cited by
- 415
- References
- 26
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 9 · 2023: 8 · 2022: 10 · 2021: 11 · 2020: 9 · 2019: 16 · 2018: 13 · 2017: 13 · 2016: 8 · 2015: 13 · 2014: 23 · 2013: 21 · 2012: 24
- FWCI
- 19.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Gut (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- National University of Singapore (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Wellcome Trust
- Royal College of Physicians and Surgeons of Glasgow
- National University of Singapore
- Canadian Institutes of Health Research
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- post-infectious irritable bowel syndrome, IL-1β, interleukin-1 receptor antagonist, rectal mucosa, intestinal inflammation, acute gastroenteritis, gene expression, rectal biopsy, psychosocial factors
- MeSH terms
- Acute Disease, Adult, Bacterial Infections, Colonic Diseases, Functional, Female, Gastroenteritis, Humans, Interleukin-1, Intestinal Mucosa, Male, Middle Aged, Prospective Studies, Rectum, RNA, Messenger, Sialoglycoproteins, Gene Expression, Genetic Predisposition to Disease, Reverse Transcriptase Polymerase Chain Reaction, Interleukin 1 Receptor Antagonist Protein
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