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

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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

DOI 10.1136/gut.2003.021154PMC PMC1774156

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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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Background
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ResultInfluential
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BackgroundResultInfluential
Irritable bowel syndrome is strongly associated with the primary and idiopathic mast cell disorders
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Ekinci, R. M. K., Balcı, S., Mart, Ö. Ö., Tümgör, G., Yavuz, S., Çelik, H., Dogruel, D., Altıntaş, D. U., & Yılmaz, M. (2018) · Rheumatology International · doi:10.1007/s00296-018-4129-7 · Cited by 11
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“Evidence suggests that an episode of acute gastroenteritis may lead to the development of IBS symptoms only if other factors favour activation of mast cells and other gastrointestinal inﬂammatory cells via psychological, neural, and endocrine mechanisms.”
Pathophysiologic Findings of Irritable Bowel Syndrome in China
Zhong, L., & Hou, X. (2012) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2012.18.1.19 · Cited by 10
“8% in controls.(70) The incidence of PI-IBS has been reported to vary from 4% to 32% worldwide in a meta-analysis, with most about 10%, which was significantly”
Influential
Immunolocalization of NOS, VIP, galanin and SP in the small intestine of suckling pigs treated with red kidney bean (Phaseolus vulgaris) lectin
Zacharko-Siembida, A., PIEDRA, J. L. V., Szymańczyk, S., & Arciszewski, M. B. (2012) · Acta Histochemica · doi:10.1016/j.acthis.2012.06.010 · Cited by 10
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Irritable Bowel Syndrome
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A Bayesian Approach to Acute Infectious Diarrhea in Adults
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High degree of duodenal inflammation in Nigerians with functional dyspepsia
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Craig, O., & Quigley, E. (2010) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/egh.10.31 · Cited by 10
Affects of ionizing radiation on T-cell population lymphocyte: A risk factor of Irritable Bowel Syndrome
Sajjadieh, M. R. S., Kuznetsova, L., & Bojenko, V. B. (2010) · Toxicology and Industrial Health · doi:10.1177/0748233710364965 · Cited by 7
“In IBS biopsies, mast cell density is increased in the intestinal mucosa, and mast cells appear closer to nerve fibers than in controls (Wang et al., 2004).”
Background
Comparative expression profiling in the intestine of patients with Giardia ‐induced postinfectious functional gastrointestinal disorders
Martínez, C., Lasitschka, F., Thöni, C., Wohlfarth, C., Braun, A., Granzow, M., Röth, R., Dizdar, V., Rappold, G., Hausken, T., et al. (2020) · Neurogastroenterology & Motility · doi:10.1111/nmo.13868 · Cited by 7
Effect of NSAIDs Supplementation on the PACAP-, SP- and GAL-Immunoreactive Neurons in the Porcine Jejunum
Brzozowska, M., Jana, B., & Całka, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111689 · Cited by 7
“The changes in SP expression within the ENS have been noted in parasite infection [15], carcinoma [16] and inflammatory bowel disease [17], while the changes in the number of GAL-like immunoreactive (LI) enteric nervous structures have been recorded after bisphenol A supplementation [18] and experimentally induced ile…”
Background
T helper cell polarisation in coeliac disease: any (T-)bet ?
Holtmann, M. H., & Neurath, M. F. (2004) · Gut · doi:10.1136/gut.2003.038232 · Cited by 7
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Editorial: A Closer Look at Mucosal Inflammation in Irritable Bowel Syndrome: Sex- and Gender-Related Disparities—Quantity, Quality, or Both?
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Post-Infectious Sequelae of Travelers’ Diarrhea: Reactive Arthritis, Guillain-Barré Syndrome, and Irritable Bowel Syndrome
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“Preliminary studies have recently identified immunologic biomarkers in patients with infectious gastroenteritis who develop PI-IBS [54, 56, 74, 88].”
Background
Tachykinin NK2 antagonist for treatments of various disease states
Jung, H. J., & Priefer, R. (2021) · Autonomic Neuroscience · doi:10.1016/j.autneu.2021.102865 · Cited by 7
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Spiller, R. E. (2005) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2005.02.001 · Cited by 6
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Sanders, J. W., Riddle, M. S., Brewster, S. J., & Taylor, D. N. (2008) · Elsevier eBooks · doi:10.1016/b978-0-323-03453-1.10016-1 · Cited by 6
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Effects of Dachengqi Decoction (大承气汤) on morphological changes in enteric nerve system of rats with multiple organ dysfunction syndrome
Xie, M.-Z., Qi, Q.-H., Zhang, S.-L., & Wei, M.-M. (2015) · Chinese Journal of Integrative Medicine · doi:10.1007/s11655-015-1978-8 · Cited by 5
Efficacy and mode of action of mesalazine in the treatment of diarrhoea-predominant irritable bowel syndrome (IBS-D): a multicentre, parallel-group, randomised placebo-controlled trial
Lam, C., Tan, W., Leighton, M., Hastings, M. C., Lingaya, M. R., Falcone, Y., Zhou, X., Xu, L., Whorwell, P. J., Walls, A. F., et al. (2015) · Efficacy and Mechanism Evaluation · doi:10.3310/eme02020 · Cited by 5
Mast Cells and Intestinal Motility Disorders (Mastocytic Enteritis/Colitis)
Schaeffer, D. F., Kirsch, R., & Riddell, R. H. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2123-6 · Cited by 5
“MC proximal to enteric nerves, previously reported in animal [24] and human studies [3, 8, 11], led to the hypothesis that psychological or physical stress may activate the enteric nervous system via the central nervous system subsequently attracting and potentially activating MC [25].”
Background
Irritable bowel syndrome – a new approach to aetiopathogenesis
Nehring, P., Mrozikiewicz‐Rakowska, B., Krasnodębski, P., & Karnafel, W. (2011) · Gastroenterology Review · doi:10.5114/pg.2011.20103 · Cited by 5
Significance of Postinfectious Irritable Bowel Syndrome?
Spiller, R. E. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.11.034 · Cited by 5
Travelers’ diarrhea: Clinical practice guidelines for pharmacists
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Mast Cell Disorders of the Gastrointestinal Tract
Panarelli, N. C. (2023) · Surgical pathology clinics · doi:10.1016/j.path.2023.05.010 · Cited by 5
T1307 Treatment of Diarrhea-Predominant Irritable Bowel Syndrome with mesalazine and/or Saccharomyces Boulardii
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Palus, K., Bulc, M., & Całka, J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249691 · Cited by 4
“SP stimulates the synthesis of TNF-α, IL-1β, and IL-6 in the human colonic mucosa [64], increases the production of IL-1β and IL-6 mRNA in human glial cells, and co-operates with mast cells in the wall of ileum and ascending colon of irritable bowel syndrome (IBS) patients [65,66].”
Background
Risk Factors of Developing Postinfectious Irritable Bowel Syndrome in Shigellosis Patients, 5 Years After Hospitalization During the Outbreak
Soheilipour, M., Chahichi, A., Mohajer, H., Ghomashi, N., Roohafza, H., & Adibi, P. (2024) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofae032 · Cited by 4
“Another study investigating 295 patients with bacillary dys-entery, of which 71.4% were Shigella cases, showed a significantly higher incidence of PI-IBS in the dysentery group compared to the controls, with age and sex having no significant impact on the development of PI-IBS [27].”
Influential
The Relationship of Enteric Microbial Infection and Functional Bowel Disorders
Collins, S. (2007) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31802db351 · Cited by 6
Gender Differences in Irritable Bowel Syndrome
Pickett‐Blakely, O., Lee, L. A., & Mullin, G. E. (2010) · Principles of Gender-Specific Medicine · doi:10.1016/b978-0-12-374271-1.00032-0 · Cited by 5
Prospective study evaluating immune‐mediated mechanisms and predisposing factors underlying persistent postinfectious abdominal complaints
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Pathogenic Factors in Postinfectious Irritable Bowel Syndrome - An Update.
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Association between Toll-like receptor 9 signaling defect and developing post-infectious irritable bowel syndrome
Kotani, S., Mishima, Y., Kishimoto, K., Oka, A., Oshima, N., Kawashima, K., Matsumoto, K., Usuda, H., Wada, K., & Ishihara, S. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1672117 · Cited by 4
“In clinical practice, enterocolitis severity is thought to be associated with development of PI-IBS (15 – 17, 67, 68).”
The evolution of irritable bowel syndrome as a group of organic diseases: a narrative review
Saidara, E., Barlow, G. M., & Pimentel, M. (2025) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2025.2549381 · Cited by 3

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
DOI: 10.1136/gut.2003.021154
PMC: PMC1774156
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: hybrid
doi.org
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
Health Sciences › Medicine › Gastroenterology › 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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Bacillary dysentery as a causative factor of irritable bowel syndrome and its pathogenesis

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