Cited by 220Gastrointestinal motility and disordersGut microbiota and healthInflammatory Bowel Disease

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The Immune System in Irritable Bowel Syndrome

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Barbara, Giovanni, Cremon, Cesare, Carini, Giovanni, Bellacosa, Lara, Zecchi, Lisa, Giorgio, Roberto De, Corinaldesi, Roberto, Stanghellini, Vincenzo·2011·Journal of Neurogastroenterology and Motility

DOI 10.5056/jnm.2011.17.4.349PMC PMC3228974

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Abstract

The potential relevance of systemic and gastrointestinal immune activation in the pathophysiology and symptom generation in the irritable bowel syndrome (IBS) is supported by a number of observations. Infectious gastroenteritis is the strongest risk factor for the development of IBS and increased rates of IBS-like symptoms have been detected in patients with inflammatory bowel disease in remission or in celiac disease patients on a gluten free diet. The number of T cells and mast cells in the small and large intestine of patients with IBS is increased in a large proportion of patients with IBS over healthy controls. Mediators released by immune cells and likely from other non-immune competent cells impact on the function of enteric and sensory afferent nerves as well as on epithelial tight junctions controlling mucosal barrier of recipient animals, isolated human gut tissues or cell culture systems. Antibodies against microbiota antigens (bacterial flagellin), and increased levels of cytokines have been detected systemically in the peripheral blood advocating the existence of abnormal host-microbial interactions and systemic immune responses. Nonetheless, there is wide overlap of data obtained in healthy controls; in addition, the subsets of patients showing immune activation have yet to be clearly identified. Gender, age, geographic differences, genetic predisposition, diet and differences in the intestinal microbiota likely play a role and further research has to be done to clarify their relevance as potential mechanisms in the described immune system dysregulation. Immune activation has stimulated interest for the potential identification of biomarkers useful for clinical and research purposes and the development of novel therapeutic approaches.

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Figure 1 Putative biological factors involved in the pathophysiology of irritable bowel syndrome. CRF, corticotropin releasing factor; SERT, serotonin reuptake transporter.CC BY-NC · PubMed Central

Figure 2 Schematic representation of translational approach to assess the impact of mucosal bioactive factors on sensory afferents, enteric nerves and epithelial permeability. (A) Mucosal biopsies are taken from the mucosa of descending colon. (B) Mucosal spontaneous release of bioactive factors is obtained, collected and stored. (C) Laboratory animals and surgical resection specimens of colon are used as recipient for the assessment of the impact of isolated mediators. (D) Readout of visceral sensitivity, sensory nerve discharge, enteric nervous system function and mucosal permeability can be assessed in the presence or absence of specific pharmacologic antagonists/inhibitors to identify specific molecules involved. IBS, irritable bowel syndrome; ENS, enteric nervous system. Adapted from Cenac et al,5 Barbara et al,6 Buhner et al8 and Piche et al.9CC BY-NC · PubMed Central

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The Role of Neuro-Immune Interaction in Chronic Pain Conditions; Functional Somatic Syndrome, Neurogenic Inflammation, and Peripheral Neuropathy
Meade, E., & Garvey, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158574 · Cited by 56
“Immune cells are known to interact with nerve tissue of the GIT in patients diagnosed with IBS, FM, IC, and vulvar vestibulitis [19].”
BackgroundInfluential
What does irritable bowel syndrome share with non-alcoholic fatty liver disease?
Scalera, A. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i33.5402 · Cited by 48
Efficacy of combination therapy with probiotics and mosapride in patients with IBS without diarrhea: a randomized, double‐blind, placebo‐controlled, multicenter, phase II trial
Choi, C. H., Kwon, J. G., Kim, S. K., Myung, S. ‐., Park, K. S., Sohn, C. ‐., Rhee, P. ‐., Lee, K. J., Lee, O. Y., Jung, H. ‐., et al. (2015) · Neurogastroenterology & Motility · doi:10.1111/nmo.12544 · Cited by 46
Genome‐wide DNA methylation profiling of peripheral blood mononuclear cells in irritable bowel syndrome
Mahurkar‐Joshi, S., Polytarchou, C., Iliopoulos, D., Pothoulakis, C., Mayer, E. A., & Chang, L. (2015) · Neurogastroenterology & Motility · doi:10.1111/nmo.12741 · Cited by 45
New and emerging therapies for the treatment of irritable bowel syndrome: an update for gastroenterologists
Foxx–Orenstein, A. E. (2016) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x16633050 · Cited by 45
Irritable Bowel Syndrome
Mullin, G. E., Shepherd, S. J., Roland, B. C., Ireton-Jones, C. S., & Matarese, L. E. (2014) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607114545329 · Cited by 47
Probiotics reduce repeated water avoidance stress-induced colonic microinflammation in Wistar rats in a sex-specific manner
Lee, J. Y., Kim, N., Nam, R. H., Sohn, S. H., Lee, S. M., Choi, D., Yoon, H., Kim, Y. S., Lee, H. S., & Lee, D. H. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188992 · Cited by 44
Early life stress in mice is a suitable model for Irritable Bowel Syndrome but does not predispose to colitis nor increase susceptibility to enteric infections
Riba, A., Olier, M., Lacroix‐Lamandé, S., Lencina, C., Bacquie, V., Harkat, C., van Langendonck, N., Gillet, M., Cartier, C., Baron, M., et al. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.05.024 · Cited by 45
“, 2014), microbiota dysbiosis (for review (Collins, 2014)) and increased state of activation of immune cells (Barbara et al., 2011) even though this last observation is still under debate.”
The Role of Diet in the Treatment of Irritable Bowel Syndrome
Singh, R., Salem, A., Nanavati, J., & Mullin, G. E. (2018) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2017.10.003 · Cited by 42
“toward visceral hypersensitivity, and is noticeable in a number of IBS subtypes (ie, postinfectious IBS, IBS-D).(31,32) Studies have suggested an association of between mast cell mediators with worsened symptoms severity and psychosocial comorbidity.”
Background
Alteration of the intestinal microbiota as a cause of and a potential therapeutic option in irritable bowel syndrome
König, J., & Brummer, R. J. (2014) · Beneficial Microbes · doi:10.3920/bm2013.0033 · Cited by 43
“Mild immune activation has been found both locally in the gut and systemically (Barbara et al. , 2011), and mucosal biopsies from IBS patients are characterised by an increased quantity of various immune cells, such as mast cells (Bischoff, 2009; Chadwick et al. , 2002; Cremon et al. , 2009).”
Increased intestinal mucosal leptin levels in patients with diarrhea-predominant irritable bowel syndrome
Liu, D.-R., Xu, X., & Yao, S. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i1.46 · Cited by 42
Alteration of Th1/Th2/Th17 cytokine profile and humoral immune responses associated with chromate exposure
Qin, Q., Li, P., Wang, T., Zhang, J., Yu, S., Chen, T., Yan, L., Song, Y., Liu, X., Gu, Y., et al. (2013) · Occupational and Environmental Medicine · doi:10.1136/oemed-2013-101421 · Cited by 40
A New Proposal for the Pathogenic Mechanism of Non-Coeliac/Non-Allergic Gluten/Wheat Sensitivity: Piecing Together the Puzzle of Recent Scientific Evidence
Leccioli, V., Oliveri, M., Romeo, M., Berretta, M., & Rossi, P. (2017) · Nutrients · doi:10.3390/nu9111203 · Cited by 39
“[119] suggested that in sensitive patients the immunological response could be greater in the colon rather than in the duodenal mucosa, because NCG/WS is generally characterized by GI symptoms also present in IBS, which is very often characterized by colonic mucosal inflammation [40,120,121].”
Background
Interleukin-10: A Compelling Therapeutic Target in Patients With Irritable Bowel Syndrome
Kumar, S., Shukla, R., Ranjan, P., & Kumar, A. (2017) · Clinical Therapeutics · doi:10.1016/j.clinthera.2017.01.030 · Cited by 38
“] 2017 of recurrent abdominal pain or discomfort, abdominal bloating, and altered bowel habits in the absence of an organic cause.(1) The prevalence of IBS varies from 4% to 20% worldwide, and IBS can have a significant negative impact on lifestyle and social well-being.”
Background
Clinical Response and Changes of Cytokines and Zonulin Levels in Patients with Diarrhoea-Predominant Irritable Bowel Syndrome Treated with Bifidobacterium Longum ES1 for 8 or 12 Weeks: A Preliminary Report
Caviglia, G. P., Tucci, A., Pellicano, R., Fagoonee, S., Rosso, C., Abate, M. L., Olivero, A., Armandi, A., Vanni, E., Saracco, G. M., et al. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9082353 · Cited by 40
“Accordingly, patients with IBS showed increased levels of pro-inflammatory cytokines including interleukin (IL)-1b, tumour necrosis factor-alpha (TNFα), IL-6 and IL-8, and reduced levels of anti-inflammatory cytokines such as IL-10 [11], IL-5 and IL-13 [10].”
Background
Mast cell‐nerve interactions correlate with bloating and abdominal pain severity in patients with non‐celiac gluten / wheat sensitivity
Giancola, F., Volta, U., Repossi, R., Latorre, R., Beeckmans, D., Carbone, F., den Houte, K. V., Bianco, F., Bonora, E., Gori, A., et al. (2020) · Neurogastroenterology & Motility · doi:10.1111/nmo.13814 · Cited by 41
Self-citation
Inflammatory cell distribution in colon mucosa as a new tool for diagnosis of irritable bowel syndrome: A promising pilot study
Boyer, J., Saint‐Paul, M., Dadone‐Montaudié, B., Patouraux, S., Vivinus, M., Ouvrier, D., Michiels, J., Piche, T., & Tulić, M. K. (2017) · Neurogastroenterology & Motility · doi:10.1111/nmo.13223 · Cited by 35
Bacillus spp. Spores—A Promising Treatment Option for Patients with Irritable Bowel Syndrome
Cătinean, A., Neag, A. M., Nita, A., Buzea, M., & Buzoianu, A. D. (2019) · Nutrients · doi:10.3390/nu11091968 · Cited by 35
Chang-Kang-Fang alleviates diarrhea predominant irritable bowel syndrome (IBS-D) through inhibiting TLR4/NF-κB/NLRP3 pathway
Zhang, S., Tian, D., Xia, Z., Yang, F., Chen, Y., Yao, Z., He, Y., Miao, X., Zhou, G., Yao, X., et al. (2024) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2024.118236 · Cited by 33
Gut–Brain Axis: Focus on Neurodegeneration and Mast Cells
Conte, C., Sichetti, M., & Traina, G. (2020) · Applied Sciences · doi:10.3390/app10051828 · Cited by 33
“IBD represents a group of inflammatory conditions of the colon and small intestine, generally assumed as a result of an uncontrolled immune response in genetically predisposed subjects following a change in microbiota (dysbiosis) [110].”
Background
Psychological stress‐induced colonic barrier dysfunction: Role of immune‐mediated mechanisms
Hattay, P., Prusator, D. K., Tran, L., & Meerveld, B. G. (2017) · Neurogastroenterology & Motility · doi:10.1111/nmo.13043 · Cited by 30
Expression of Neurotrophic Factors, Tight Junction Proteins, and Cytokines According to the Irritable Bowel Syndrome Subtype and Sex
Lee, J. Y., Kim, N., Park, J. H., Nam, R. H., Lee, S. M., Song, C., Kim, G., Na, H. Y., Choi, Y. J., Kim, J. J., et al. (2019) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm19099 · Cited by 31
“The possible pathophysiology of IBS is multifactorial.(6,11) Among them, emerging data highlight that neurotrophic factors and altered intestinal permeability might contribute to IBS and related symptoms.”
Background
Association between Irritable Bowel Syndrome and Allergic Diseases: To Make a Case for Aeroallergen
Loo, E. X. L., Wang, D. Y., & Siah, K. T. H. (2019) · International Archives of Allergy and Immunology · doi:10.1159/000503629 · Cited by 31
Postinfectious Functional Gastrointestinal Disorders
Mearin, F. (2011) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31821fbf58 · Cited by 30
The role of diet in the management of irritable bowel syndrome: a focus on FODMAPs
Dolan, R. D., Chey, W. D., & Eswaran, S. L. (2018) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2018.1476138 · Cited by 30
“levels [15] are now thought to contribute to the complex pathogenesis of IBS.”
Background
IBS clinical management in Italy: The AIGO survey
Soncini, M., Stasi, C., Usai–Satta, P., Milazzo, G., Bianco, M., Leandro, G., Montalbano, L. M., Muscatiello, N., Monica, F., Galeazzi, F., et al. (2018) · Digestive and Liver Disease · doi:10.1016/j.dld.2018.10.006 · Cited by 30
Gastrointestinal neuromuscular apparatus: An underestimated target of gut microbiota
Guarino, M. P. L., Cicala, M., Putignani, L., & Severi, C. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i45.9871 · Cited by 29
Neuropsychological function is related to irritable bowel syndrome in women with premenstrual syndrome and dysmenorrhea
Ayadilord, M., Mahmoudzadeh, S., Hoseini, Z. S., Askari, M., Rezapour, H., Saharkhiz, M., Abbaszadeh, A., Karbasi, S., Dasht-e-Bayaz, N. Z., Ferns, G. A., et al. (2020) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-020-05659-3 · Cited by 26
Increased fermentable carbohydrate intake alters colonic mucus barrier function through glycation processes and increased mast cell counts
Kamphuis, J. B. J., Reber, L. L., Eutamène, H., & Théodorou, V. (2022) · The FASEB Journal · doi:10.1096/fj.202100494rrr · Cited by 27
Repeated Water Avoidance Stress Alters Mucosal Mast Cell Counts, Interleukin-1β Levels with Sex Differences in the Distal Colon of Wistar Rats
Lee, J. Y., Kim, N., Kim, Y. S., Nam, R. H., Ham, M. H., Lee, H. S., Jo, W., Shim, Y. K., Choi, Y. J., Yoon, H., et al. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16007 · Cited by 27
“The possible pathogeneses of IBS includes stress, increased mucosal permeability, mucosal immune activation, food hypersensitivity, transient infection altering intestinal microbiota, neuroplasticity, altered enteroendocrine metabolism, and genetic polymorphisms.(2,3) Among these, stress is a key factor in the onset,…”
Background
A Randomized Clinical Trial of Synbiotics in Irritable Bowel Syndrome: Dose-Dependent Effects on Gastrointestinal Symptoms and Fatigue
Lee, S.-H., Cho, D., Lee, S., Han, K.-S., Yang, S.-W., Kim, J.-H., Lee, S.-H., Kim, S.-M., & Kim, K.-N. (2018) · Korean Journal of Family Medicine · doi:10.4082/kjfm.17.0064 · Cited by 29
Relationship Between Systemic Immune-Inflammation Index and Irritable Bowel Syndrome
Güven, İ. E., Başpınar, B., & Atalay, R. (2022) · The Turkish Journal of Gastroenterology · doi:10.5152/tjg.2021.21321 · Cited by 26
The Effect of Vitamin D Supplementation on the Severity of Symptoms and the Quality of Life in Irritable Bowel Syndrome Patients: A Systematic Review and Meta-Analysis of Randomized Controlled Trials
Abuelazm, M. T., Shoaib, M., Gamal, M., Labieb, F., Amin, M. A., Abdelazeem, B., & Brašić, J. R. (2022) · Nutrients · doi:10.3390/nu14132618 · Cited by 26
“In the pathogenesis of IBS, immunological and inflammatory roles are of particular importance as literature has emphasized the activation of the inflammatory mediator to have a crucial part in the IBS development [46].”
Background
The role of intestinal mast cell infiltration in irritable bowel syndrome
Cheng, L., Luo, Q., & Chen, S. (2021) · Journal of Digestive Diseases · doi:10.1111/1751-2980.12971 · Cited by 25
Role of microRNAs in Disorders of Gut–Brain Interactions: Clinical Insights and Therapeutic Alternatives
Singh, R., Zogg, H., & Ro, S. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11101021 · Cited by 25
Oligo-Antigenic Diet in the Treatment of Chronic Anal Fissures. Evidence for a Relationship Between Food Hypersensitivity and Anal Fissures
Carroccio, A., Mansueto, P., Morfino, G., D’Alcamo, A., Paola, V. D., Iacono, G., Soresi, M., Scerrino, G., Maresi, E., Gulotta, G., et al. (2013) · The American Journal of Gastroenterology · doi:10.1038/ajg.2013.58 · Cited by 25
Association between gastrointestinal motility and macrophage/mast cell distribution in mice during the healing stage after DSS‑induced colitis
Kodani, M., Fukui, H., Tomita, T., Oshima, T., Watari, J., & Miwa, H. (2018) · Molecular Medicine Reports · doi:10.3892/mmr.2018.8926 · Cited by 23
“Among immune cells, mast cell is highlighted in the pathophysiology of IBS since the number of mast cells is increased in the colonic tissues in patients with IBS and moreover correlated with the severity of their clinical symptoms (8,9).”
Aberrant Gut-To-Brain Signaling in Irritable Bowel Syndrome - The Role of Bile Acids
Dhonnabháín, R. N., Xiao, Q., & O’Malley, D. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.745190 · Cited by 25
“In addition to genetic, epigenetic (47), immunological (48), gender differences (49) and food hypersensitivity (50, 51) being reported in individuals with IBS, an increased prevalence of adverse life events and comorbid mood disorders such as anxiety, depression and somatoform disorders (52, 53) are also common.”
Background
Role of inflammation in pediatric irritable bowel syndrome
Nardo, G. D., Cremon, C., Staiano, A., Stanghellini, V., Borrelli, O., Strisciuglio, C., Romano, C., Mallardo, S., Scarpato, E., Marasco, G., et al. (2022) · Neurogastroenterology & Motility · doi:10.1111/nmo.14365 · Cited by 21
Self-citation
Factor V Leiden and Inflammation
Pérez‐Pujol, S., Aras, Ö., & Escolar, G. (2012) · Thrombosis · doi:10.1155/2012/594986 · Cited by 21
“The inflammatory process in IBD is probably associated to an immune reaction of the body against its own vascular tissue [91].”
Background
The Protective Effect of Roseburia faecis Against Repeated Water Avoidance Stress-induced Irritable Bowel Syndrome in a Wister Rat Model
Choi, S. I., Kim, N., Nam, R. H., Jang, J. Y., Kim, E. H., Ha, S., Kang, K. S., Lee, W., Choi, H., Kim, Y.-R., et al. (2023) · Journal of Cancer Prevention · doi:10.15430/jcp.2023.28.3.93 · Cited by 24
“The etiology of IBS is multifaceted, encompassing stress, increased mucosal permeability, mucosal immune activation, food hypersensitivity, transient infection-altering intestinal microbiota, neuroplasticity, altered enteroendocrine metabolism, and genetic polymorphisms [2].”
Background
Multi-target Treatment for Irritable Bowel Syndrome with STW 5: Pharmacological Modes of Action
Allescher, H., Burgell, R., Malfertheiner, P., & Mearin, F. (2020) · Journal of Gastrointestinal and Liver Diseases · doi:10.15403/jgld-814 · Cited by 19
“This micro-inflammation may affect changes in motility and visceral sensitivity, and evoke symptoms of IBS [40].”
Background
Stem Cells in the Intestine: Possible Roles in Pathogenesis of Irritable Bowel Syndrome
Ratanasirintrawoot, S., & Israsena, N. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16023 · Cited by 19
Functional Gastrointestinal Disorders.
Duffy, M., Boggiano, V. L., Ganesh, R., & Mueller, M. (2023) · Primary Care · doi:10.1016/j.pop.2023.03.006 · Cited by 13
Low prevalence of ‘classical’ microscopic colitis but evidence of microscopic inflammation in Asian Irritable Bowel Syndrome patients with diarrhoea
Hilmi, I. N., Hartono, J. L., Pailoor, J., Mahadeva, S., & Goh, K. (2013) · BMC Gastroenterology · doi:10.1186/1471-230x-13-80 · Cited by 18
“; licensee BioMed Central L Commons Attribution License (http://creativec reproduction in any medium, provided the or psychological association [5-7].”
Background

Authors: Barbara, G., Cremon, C., Carini, G., Bellacosa, L., Zecchi, L., Giorgio, R. D., Corinaldesi, R., & Stanghellini, V.
Affiliations: University of Bologna (IT)
Corresponding author: Barbara, Giovanni
ORCID: Barbara, Giovanni
Cremon, Cesare
Carini, Giovanni
Giorgio, Roberto De
Stanghellini, Vincenzo
Venue: Journal of Neurogastroenterology and Motility
Publisher: The Korean Society of Neurogastroenterology and Motility
Published: 2011-10-31
Volume: 17
Issue: 4
Pages: 349-359
ISSN: 2093-0879 (ISSN-L)
2093-0887
DOI: 10.5056/jnm.2011.17.4.349
PMC: PMC3228974
OpenAlex: W2154410960
Cited by: 211
References: 91
Citations by year: 2026: 8 · 2025: 10 · 2024: 9 · 2023: 10 · 2022: 15 · 2021: 10 · 2020: 21 · 2019: 13 · 2018: 20 · 2017: 15 · 2016: 20 · 2015: 12 · 2014: 18 · 2013: 17 · 2012: 12
FWCI: 15.76
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
Locations: Journal of Neurogastroenterology and Motility (publishedVersion, cc-by-nc)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
Institutional Research Information System University of Ferrara (University of Ferrara) (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: irritable bowel syndrome, immune activation, gut microbiota, T cells, mast cells, enteric nerves, tight junctions, mucosal barrier, host-microbe interactions, inflammatory bowel disease, celiac disease, gluten-free diet, infectious gastroenteritis, cytokines, biomarkers, immune dysregulation

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The Immune System in Irritable Bowel Syndrome

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