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Chronic colitis-induced visceral pain is associated with increased anxiety during quiescent phase.

Abstract

Inflammatory bowel diseases (IBD) are characterized by repetition of flares and remission periods leading to chronic postinflammatory sequelae. Among postinflammatory sequelae, one-third of patients with IBD are suffering from functional symptoms or psychological comorbidities that persist during remission. The aim of our study was to assess functional and behavioral sequelae of chronic colitis in rats with quiescent intestinal inflammation. Chronic colitis was induced by a weekly intrarectal injection of increasing concentrations of trinitrobenzene sulfonic acid (TNBS) for 3 wk (15-45 mg of TNBS) in 30 rats, whereas the control rats (n = 24) received the vehicle. At 50 days post-TNBS, visceral sensitivity was assessed by visceromotor response to colorectal distension, and transient receptor potential vanilloid type 1 (TRPV1) expression was also quantified in the colon and dorsal root ganglia. Barrier function and inflammatory response were assessed by studying intestinal permeability, tight junction protein, myeloperoxidase activity, histological score, and cytokine production (IL-6, IL-10, and TNF-α). Anxiety behavioral tests were performed from 50 to 64 days after the last TNBS injection. Chronic TNBS induced 1) a visceral hypersensitivity (P = 0.03), 2) an increased colon weight-to-length ratio (P = 0.01), 3) higher inflammatory and fibrosis scores (P = 0.0390 and P = 0.0016, respectively), and 4) a higher colonic IL-6 and IL-10 production (P = 0.008 and P = 0.005, respectively) compared with control rats. Intestinal permeability, colonic production of TNF-α, myeloperoxidase activity, and TRPV1 expression did not differ among groups. Chronic TNBS increased anxiety-related behavior in the open-field test and in the acoustic stress test. In conclusion, chronic colitis induced functional sequelae such as visceral hypersensitivity and increased anxiety with a low-grade intestinal inflammation. Development of a representative animal model will allow defining novel therapeutic approaches to achieve a better management of IBD-related sequelae. NEW & NOTEWORTHY Patients with inflammatory bowel diseases have impaired quality of life. Therapeutic progress to control mucosal inflammation provides us an opportunity to develop novel approaches to understand mechanisms behind postinflammatory sequelae. We used a chronic colitis model to study long-term sequelae on visceral pain, gut barrier function, and psychological impact. Chronic colitis induced functional symptoms and increased anxiety in the remission period. It might define novel therapeutic approaches to achieve a better inflammatory bowel disease-related sequelae management.

Authors+Show Affiliations

Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France.Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France.Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France. Digestive Physiology Department, Charles Nicolle Hospital, Rouen University Hospital , Rouen , France.Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France. Behavioural Analysis Platform (Service Commun d'Analyse Comportementale), Institute for Research and Innovation in Biomedicine, University of Rouen-Normandy , Normandy , France.Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France. Behavioural Analysis Platform (Service Commun d'Analyse Comportementale), Institute for Research and Innovation in Biomedicine, University of Rouen-Normandy , Normandy , France.Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France.Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France.Department of Pathology, Charles Nicolle Hospital, Rouen University Hospital , Rouen , France.Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France.Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France. Department of Nutrition, Charles Nicolle Hospital, Rouen University Hospital , Rouen , France.Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France. Gastroenterology Unit, Charles Nicolle Hospital, Rouen University Hospital , Rouen , France.Institut National de la Santé et de la Recherche Médicale Unit 1073 "Digestive Tract Environment and Nutrition," Normandie University, UNIROUEN, France. Institute for Research and Innovation in Biomedicine, Normandie University, Union Nationale Inter-Universitaire Rouen , Rouen , France.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

30735453

Citation

Salameh, Emmeline, et al. "Chronic Colitis-induced Visceral Pain Is Associated With Increased Anxiety During Quiescent Phase." American Journal of Physiology. Gastrointestinal and Liver Physiology, vol. 316, no. 6, 2019, pp. G692-G700.
Salameh E, Meleine M, Gourcerol G, et al. Chronic colitis-induced visceral pain is associated with increased anxiety during quiescent phase. Am J Physiol Gastrointest Liver Physiol. 2019;316(6):G692-G700.
Salameh, E., Meleine, M., Gourcerol, G., do Rego, J. C., do Rego, J. L., Legrand, R., ... Marion-Letellier, R. (2019). Chronic colitis-induced visceral pain is associated with increased anxiety during quiescent phase. American Journal of Physiology. Gastrointestinal and Liver Physiology, 316(6), pp. G692-G700. doi:10.1152/ajpgi.00248.2018.
Salameh E, et al. Chronic Colitis-induced Visceral Pain Is Associated With Increased Anxiety During Quiescent Phase. Am J Physiol Gastrointest Liver Physiol. 2019 Jun 1;316(6):G692-G700. PubMed PMID: 30735453.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Chronic colitis-induced visceral pain is associated with increased anxiety during quiescent phase. AU - Salameh,Emmeline, AU - Meleine,Mathieu, AU - Gourcerol,Guillaume, AU - do Rego,Jean-Claude, AU - do Rego,Jean-Luc, AU - Legrand,Romain, AU - Breton,Jonathan, AU - Aziz,Moutaz, AU - Guérin,Charlène, AU - Coëffier,Moïse, AU - Savoye,Guillaume, AU - Marion-Letellier,Rachel, Y1 - 2019/02/08/ PY - 2019/2/9/pubmed PY - 2019/2/9/medline PY - 2019/2/9/entrez KW - anxiety KW - chronic colitis KW - intestinal permeability KW - visceral hypersensitivity SP - G692 EP - G700 JF - American journal of physiology. Gastrointestinal and liver physiology JO - Am. J. Physiol. Gastrointest. Liver Physiol. VL - 316 IS - 6 N2 - Inflammatory bowel diseases (IBD) are characterized by repetition of flares and remission periods leading to chronic postinflammatory sequelae. Among postinflammatory sequelae, one-third of patients with IBD are suffering from functional symptoms or psychological comorbidities that persist during remission. The aim of our study was to assess functional and behavioral sequelae of chronic colitis in rats with quiescent intestinal inflammation. Chronic colitis was induced by a weekly intrarectal injection of increasing concentrations of trinitrobenzene sulfonic acid (TNBS) for 3 wk (15-45 mg of TNBS) in 30 rats, whereas the control rats (n = 24) received the vehicle. At 50 days post-TNBS, visceral sensitivity was assessed by visceromotor response to colorectal distension, and transient receptor potential vanilloid type 1 (TRPV1) expression was also quantified in the colon and dorsal root ganglia. Barrier function and inflammatory response were assessed by studying intestinal permeability, tight junction protein, myeloperoxidase activity, histological score, and cytokine production (IL-6, IL-10, and TNF-α). Anxiety behavioral tests were performed from 50 to 64 days after the last TNBS injection. Chronic TNBS induced 1) a visceral hypersensitivity (P = 0.03), 2) an increased colon weight-to-length ratio (P = 0.01), 3) higher inflammatory and fibrosis scores (P = 0.0390 and P = 0.0016, respectively), and 4) a higher colonic IL-6 and IL-10 production (P = 0.008 and P = 0.005, respectively) compared with control rats. Intestinal permeability, colonic production of TNF-α, myeloperoxidase activity, and TRPV1 expression did not differ among groups. Chronic TNBS increased anxiety-related behavior in the open-field test and in the acoustic stress test. In conclusion, chronic colitis induced functional sequelae such as visceral hypersensitivity and increased anxiety with a low-grade intestinal inflammation. Development of a representative animal model will allow defining novel therapeutic approaches to achieve a better management of IBD-related sequelae. NEW & NOTEWORTHY Patients with inflammatory bowel diseases have impaired quality of life. Therapeutic progress to control mucosal inflammation provides us an opportunity to develop novel approaches to understand mechanisms behind postinflammatory sequelae. We used a chronic colitis model to study long-term sequelae on visceral pain, gut barrier function, and psychological impact. Chronic colitis induced functional symptoms and increased anxiety in the remission period. It might define novel therapeutic approaches to achieve a better inflammatory bowel disease-related sequelae management. SN - 1522-1547 UR - https://www.unboundmedicine.com/medline/citation/30735453/Chronic_colitis_induced_visceral_pain_is_associated_with_increased_anxiety_during_quiescent_phase_ L2 - http://www.physiology.org/doi/full/10.1152/ajpgi.00248.2018?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -