Cited by 387Gastrointestinal motility and disordersGut microbiota and healthInflammatory Bowel Disease

Bacillary dysentery as a causative factor of irritable bowel syndrome and its pathogenesis

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Wang, L-H, Fang, X-C, Pan, G-Z·2004·Gut

Abstract

Background and aims: The incidence of irritable bowel syndrome (IBS) or functional bowel disorders (FBD) after bacillary dysentery (BD) has not been extensively evaluated, and little is known of the pathogenesis of post-infective (PI) IBS. Therefore, we investigated the incidence of IBS and FBD in a Chinese patient population who had recovered from BD. To further elucidate its pathogenesis, neuroimmunological changes, including interleukins (IL), mast cells, neuropeptides, and the relationship between mast cells and intestinal nerves, were investigated. Methods: A cohort study of 295 patients who had recovered from BD (shigella identified from stool in 71.4%) and 243 control subjects consisting of patient siblings or spouses who had not been infected with BD were included in the study. All subjects were followed up using questionnaires for 1–2 years to explore the incidence of FBD and IBS, as defined by the Rome II criteria. In 56 cases of IBS (PI and non-PI) from another source, the number of mast cells in biopsy specimens from the intestinal mucosa were stained with antitryptase antibody and counted under light microscopy. Also, the relationship of mast cells to neurone specific enolase (NSE), substance P (SP), 5-hydroxytryptamine (5-HT), or calcitonin gene related peptide positive nerve fibres was observed using double staining with alcian blue and neuropeptide antibodies. In 30 cases of IBS (PI-IBS, n = 15) taken at random from the 56 cases, expression of interleukin (IL)-1α, IL-1β, and IL-1 receptor antagonist (IL-1ra) mRNAs in intestinal mucosa were identified using reverse transcription-polymerase chain reaction. The above results were compared with 12 non-IBS controls. Results: In the BD infected cohort, the incidences of FBD and IBS were 22.4% and 8.1% (in total)–10.2% (among those in who shigella were identified) respectively, which were significantly higher (p<0.01) than the incidences of FBD (7.4%) and IBS (0.8%) in the control cohort. A longer duration of diarrhoea (⩾7 days) was associated with a higher risk of developing FBD (odds ratio 3.49 (95% confidence interval 1.71–7.13)). Expression of IL-1β mRNA in terminal ileum and rectosigmoid mucosa was significantly higher in PI-IBS patients (p<0.01). The number of mast cells in the terminal ileum mucosa in PI-IBS (11.19 (2.83)) and non-PI-IBS patients (10.78 (1.23)) was significantly increased compared with that (6.05 (0.51)) in control subjects (p<0.01). Also, in the terminal ileum and rectosigmoid mucosa of IBS patients, the density of NSE, SP, and 5-HT positively stained nerve fibres increased (p<0.05) and appeared in clusters, surrounding an increased number of mast cells (p<0.01 compared with controls). Conclusions: BD is a causative factor in PI-IBS. The immune and nervous system may both play important roles in the pathogenesis of PI-IBS.

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  • Several studies have demonstrated increased concentrations of activated mast cells in patients with IBS compared with controls.

    “Several studies have demonstrated increased concentrations of activated mast cells in patients with IBS compared with controls (11, 13, 24, 46, 89, 94, 121, 187).”
  • Some studies demonstrated an increase in activated mast cells in biopsies from specific regions of the GI tract (cecum and terminal ileum) but not from other regions, whereas other studies found activated mast cells in the descending colon.

    “Notably, some studies demonstrated an increase in activated mast cells in biopsies from specific regions of the GI tract (i.e., cecum and terminal ileum) but not from other regions (e.g., ascending colon, descending colon, rectum) (89, 121, 187), whereas other studies have found activated mast cells in the descending colon (11, 13).”
  • Levels of interleukin-1β mRNA may be increased in the small intestine, colon, and rectum of patients with PI-IBS compared with healthy controls.

    “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.”
  • In patients with PI-IBS, activation of the GI immune system follows acute GI infection.

    “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)”

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Authors
Wang, L.-H., Fang, X.-C., & Pan, G.-Z.
Affiliations
Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
Corresponding author
Pan, G-Z
Venue
Gut
Publisher
BMJ
Published
2004-07-09
Volume
53
Issue
8
Pages
1096-1101
ISSN
  • 0017-5749 (ISSN-L)
  • 1468-3288
OpenAlex
W2158018898
Cited by
387
References
51
Citations by year
2026: 5 · 2025: 5 · 2024: 3 · 2023: 8 · 2022: 3 · 2021: 9 · 2020: 10 · 2019: 17 · 2018: 17 · 2017: 18 · 2016: 19 · 2015: 19 · 2014: 31 · 2013: 18 · 2012: 23
FWCI
19.91
Type
journal article
Language
en
Open access
Licence
other-oa
Locations
  • Gut (publishedVersion, other-oa)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HighWire Press Open Archive (submittedVersion)
Topics
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
Keywords
shigellosis, irritable bowel syndrome, functional bowel disorders, Shigella, mast cells, neuroimmunology, substance P, calcitonin gene-related peptide, serotonin, interleukin-1, interleukin-1 receptor antagonist, intestinal nerves, pathogenesis, diarrhea duration
MeSH terms
Adult, Colonic Diseases, Functional, Diarrhea, Dysentery, Bacillary, Female, Follow-Up Studies, Humans, Interleukin-1, Intestinal Mucosa, Male, Mast Cells, Nerve Fibers, Phosphopyruvate Hydratase, Risk Factors, Serotonin, Substance P, Calcitonin Gene-Related Peptide, Irritable Bowel Syndrome

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