Functional bowel symptoms in quiescent inflammatory bowel diseases: Role of epithelial barrier disruption and low-grade inflammation

M. Vivinus-Nébot, G. Frin-Mathy, H. Bzioueche, R. Dainese, G. Bernard, R. Anty, J. Filippi, M. C. Saint-Paul, M. K. Tulic, V. Verhasselt, X. Hébuterne, Thierry Piche

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Abstract

Objective: To determine the role of colonic barrier defects and low-grade inflammation in irritable bowel syndrome (IBS)-like symptoms in quiescent inflammatory bowel disease (IBD). Design: Caecal biopsies were collected from 51 IBS, 49 quiescent IBD (31 Crohn's disease (CD) and 18 ulcerative colitis (UC)) patients and 27 controls. IBS was assessed using the Rome III criteria and the IBS severity score. Epithelial barrier integrity was evaluated by determining the paracellular permeability of biopsies mounted in Ussing chambers and the mRNA expression of tight junction proteins (ZO-1, α-catenin and occludin). Low-grade inflammation was evaluated by counting cells, including intraepithelial lymphocytes (IELs), eosinophils and mast cells, and by determining the mRNA and protein expression of tumour necrosis factor (TNF)-α in biopsies and culture supernatants. Results: IBS-like symptoms were present in 35.4 and 38% of CD and UC patients, respectively. Paracellular permeability was significantly increased in both quiescent IBD with IBS-like symptoms and IBS compared with quiescent IBD without IBS-like symptoms (p<0.01, respectively) or controls (p<0.01, respectively). Significantly lower expression of ZO-1 and α-catenin was detected in IBS and quiescent IBD with IBS-like symptoms. IELs and TNF-α were significantly increased in quiescent IBD with IBS-like symptoms, but not in IBS. Conclusions: In quiescent IBD, IBS-like symptoms related to persistent subclinical inflammation associated with increased colonic paracellular permeability. A persistent increase in TNF-α in colonic mucosa may contribute to the epithelial barrier defects associated with abdominal pain in quiescent IBD, but not in IBS. Optimisation of anti-inflammatory therapy may be considered in quiescent IBD with IBS-like symptoms.

Original languageEnglish
Pages (from-to)744-752
Number of pages9
JournalGut
Volume63
Issue number5
DOIs
Publication statusPublished - 1 May 2014
Externally publishedYes

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Irritable Bowel Syndrome
Inflammatory Bowel Diseases
Inflammation
Catenins
Permeability
Tumor Necrosis Factor-alpha
Ulcerative Colitis
Biopsy
Crohn Disease
Zonula Occludens-1 Protein
Lymphocytes
Occludin
Messenger RNA
Eosinophils
Mast Cells
Abdominal Pain

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Vivinus-Nébot, M., Frin-Mathy, G., Bzioueche, H., Dainese, R., Bernard, G., Anty, R., ... Piche, T. (2014). Functional bowel symptoms in quiescent inflammatory bowel diseases: Role of epithelial barrier disruption and low-grade inflammation. Gut, 63(5), 744-752. https://doi.org/10.1136/gutjnl-2012-304066
Vivinus-Nébot, M. ; Frin-Mathy, G. ; Bzioueche, H. ; Dainese, R. ; Bernard, G. ; Anty, R. ; Filippi, J. ; Saint-Paul, M. C. ; Tulic, M. K. ; Verhasselt, V. ; Hébuterne, X. ; Piche, Thierry. / Functional bowel symptoms in quiescent inflammatory bowel diseases : Role of epithelial barrier disruption and low-grade inflammation. In: Gut. 2014 ; Vol. 63, No. 5. pp. 744-752.
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abstract = "Objective: To determine the role of colonic barrier defects and low-grade inflammation in irritable bowel syndrome (IBS)-like symptoms in quiescent inflammatory bowel disease (IBD). Design: Caecal biopsies were collected from 51 IBS, 49 quiescent IBD (31 Crohn's disease (CD) and 18 ulcerative colitis (UC)) patients and 27 controls. IBS was assessed using the Rome III criteria and the IBS severity score. Epithelial barrier integrity was evaluated by determining the paracellular permeability of biopsies mounted in Ussing chambers and the mRNA expression of tight junction proteins (ZO-1, α-catenin and occludin). Low-grade inflammation was evaluated by counting cells, including intraepithelial lymphocytes (IELs), eosinophils and mast cells, and by determining the mRNA and protein expression of tumour necrosis factor (TNF)-α in biopsies and culture supernatants. Results: IBS-like symptoms were present in 35.4 and 38{\%} of CD and UC patients, respectively. Paracellular permeability was significantly increased in both quiescent IBD with IBS-like symptoms and IBS compared with quiescent IBD without IBS-like symptoms (p<0.01, respectively) or controls (p<0.01, respectively). Significantly lower expression of ZO-1 and α-catenin was detected in IBS and quiescent IBD with IBS-like symptoms. IELs and TNF-α were significantly increased in quiescent IBD with IBS-like symptoms, but not in IBS. Conclusions: In quiescent IBD, IBS-like symptoms related to persistent subclinical inflammation associated with increased colonic paracellular permeability. A persistent increase in TNF-α in colonic mucosa may contribute to the epithelial barrier defects associated with abdominal pain in quiescent IBD, but not in IBS. Optimisation of anti-inflammatory therapy may be considered in quiescent IBD with IBS-like symptoms.",
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Vivinus-Nébot, M, Frin-Mathy, G, Bzioueche, H, Dainese, R, Bernard, G, Anty, R, Filippi, J, Saint-Paul, MC, Tulic, MK, Verhasselt, V, Hébuterne, X & Piche, T 2014, 'Functional bowel symptoms in quiescent inflammatory bowel diseases: Role of epithelial barrier disruption and low-grade inflammation' Gut, vol. 63, no. 5, pp. 744-752. https://doi.org/10.1136/gutjnl-2012-304066

Functional bowel symptoms in quiescent inflammatory bowel diseases : Role of epithelial barrier disruption and low-grade inflammation. / Vivinus-Nébot, M.; Frin-Mathy, G.; Bzioueche, H.; Dainese, R.; Bernard, G.; Anty, R.; Filippi, J.; Saint-Paul, M. C.; Tulic, M. K.; Verhasselt, V.; Hébuterne, X.; Piche, Thierry.

In: Gut, Vol. 63, No. 5, 01.05.2014, p. 744-752.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Functional bowel symptoms in quiescent inflammatory bowel diseases

T2 - Role of epithelial barrier disruption and low-grade inflammation

AU - Vivinus-Nébot, M.

AU - Frin-Mathy, G.

AU - Bzioueche, H.

AU - Dainese, R.

AU - Bernard, G.

AU - Anty, R.

AU - Filippi, J.

AU - Saint-Paul, M. C.

AU - Tulic, M. K.

AU - Verhasselt, V.

AU - Hébuterne, X.

AU - Piche, Thierry

PY - 2014/5/1

Y1 - 2014/5/1

N2 - Objective: To determine the role of colonic barrier defects and low-grade inflammation in irritable bowel syndrome (IBS)-like symptoms in quiescent inflammatory bowel disease (IBD). Design: Caecal biopsies were collected from 51 IBS, 49 quiescent IBD (31 Crohn's disease (CD) and 18 ulcerative colitis (UC)) patients and 27 controls. IBS was assessed using the Rome III criteria and the IBS severity score. Epithelial barrier integrity was evaluated by determining the paracellular permeability of biopsies mounted in Ussing chambers and the mRNA expression of tight junction proteins (ZO-1, α-catenin and occludin). Low-grade inflammation was evaluated by counting cells, including intraepithelial lymphocytes (IELs), eosinophils and mast cells, and by determining the mRNA and protein expression of tumour necrosis factor (TNF)-α in biopsies and culture supernatants. Results: IBS-like symptoms were present in 35.4 and 38% of CD and UC patients, respectively. Paracellular permeability was significantly increased in both quiescent IBD with IBS-like symptoms and IBS compared with quiescent IBD without IBS-like symptoms (p<0.01, respectively) or controls (p<0.01, respectively). Significantly lower expression of ZO-1 and α-catenin was detected in IBS and quiescent IBD with IBS-like symptoms. IELs and TNF-α were significantly increased in quiescent IBD with IBS-like symptoms, but not in IBS. Conclusions: In quiescent IBD, IBS-like symptoms related to persistent subclinical inflammation associated with increased colonic paracellular permeability. A persistent increase in TNF-α in colonic mucosa may contribute to the epithelial barrier defects associated with abdominal pain in quiescent IBD, but not in IBS. Optimisation of anti-inflammatory therapy may be considered in quiescent IBD with IBS-like symptoms.

AB - Objective: To determine the role of colonic barrier defects and low-grade inflammation in irritable bowel syndrome (IBS)-like symptoms in quiescent inflammatory bowel disease (IBD). Design: Caecal biopsies were collected from 51 IBS, 49 quiescent IBD (31 Crohn's disease (CD) and 18 ulcerative colitis (UC)) patients and 27 controls. IBS was assessed using the Rome III criteria and the IBS severity score. Epithelial barrier integrity was evaluated by determining the paracellular permeability of biopsies mounted in Ussing chambers and the mRNA expression of tight junction proteins (ZO-1, α-catenin and occludin). Low-grade inflammation was evaluated by counting cells, including intraepithelial lymphocytes (IELs), eosinophils and mast cells, and by determining the mRNA and protein expression of tumour necrosis factor (TNF)-α in biopsies and culture supernatants. Results: IBS-like symptoms were present in 35.4 and 38% of CD and UC patients, respectively. Paracellular permeability was significantly increased in both quiescent IBD with IBS-like symptoms and IBS compared with quiescent IBD without IBS-like symptoms (p<0.01, respectively) or controls (p<0.01, respectively). Significantly lower expression of ZO-1 and α-catenin was detected in IBS and quiescent IBD with IBS-like symptoms. IELs and TNF-α were significantly increased in quiescent IBD with IBS-like symptoms, but not in IBS. Conclusions: In quiescent IBD, IBS-like symptoms related to persistent subclinical inflammation associated with increased colonic paracellular permeability. A persistent increase in TNF-α in colonic mucosa may contribute to the epithelial barrier defects associated with abdominal pain in quiescent IBD, but not in IBS. Optimisation of anti-inflammatory therapy may be considered in quiescent IBD with IBS-like symptoms.

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U2 - 10.1136/gutjnl-2012-304066

DO - 10.1136/gutjnl-2012-304066

M3 - Article

VL - 63

SP - 744

EP - 752

JO - Gut: an international journal of gastroenterology & hepatology

JF - Gut: an international journal of gastroenterology & hepatology

SN - 0017-5749

IS - 5

ER -