Cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement

Abstract Background There is growing recognition that bidirectional signaling between the digestive tract and the brain contributes to irritable bowel syndrome (IBS). We recently showed in a large randomized controlled trial that cognitive behavioral therapy (CBT) reduces IBS symptom severity. This...

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Autores principales:	Jonathan P. Jacobs, Arpana Gupta, Ravi R. Bhatt, Jacob Brawer, Kan Gao, Kirsten Tillisch, Venu Lagishetty, Rebecca Firth, Gregory D. Gudleski, Benjamin M. Ellingson, Jennifer S. Labus, Bruce D. Naliboff, Jeffrey M. Lackner, Emeran A. Mayer
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Cognitive behavioral therapy Irritable bowel syndrome Brain-gut-microbiome axis Neuroimaging Biomarkers Outcome prediction Microbial ecology QR100-130
Acceso en línea:	https://doaj.org/article/9211767c78c54222a359b868989af16a
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spelling	oai:doaj.org-article:9211767c78c54222a359b868989af16a2021-12-05T12:07:03ZCognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement10.1186/s40168-021-01188-62049-2618https://doaj.org/article/9211767c78c54222a359b868989af16a2021-11-01T00:00:00Zhttps://doi.org/10.1186/s40168-021-01188-6https://doaj.org/toc/2049-2618Abstract Background There is growing recognition that bidirectional signaling between the digestive tract and the brain contributes to irritable bowel syndrome (IBS). We recently showed in a large randomized controlled trial that cognitive behavioral therapy (CBT) reduces IBS symptom severity. This study investigated whether baseline brain and gut microbiome parameters predict CBT response and whether response is associated with changes in the brain-gut-microbiome (BGM) axis. Methods Eighty-four Rome III-diagnosed IBS patients receiving CBT were drawn from the Irritable Bowel Syndrome Outcome Study (IBSOS; ClinicalTrials.gov NCT00738920) for multimodal brain imaging and psychological assessments at baseline and after study completion. Fecal samples were collected at baseline and post-treatment from 34 CBT recipients for 16S rRNA gene sequencing, untargeted metabolomics, and measurement of short-chain fatty acids. Clinical measures, brain functional connectivity and microstructure, and microbiome features associated with CBT response were identified by multivariate linear and negative binomial models. Results At baseline, CBT responders had increased fecal serotonin levels, and increased Clostridiales and decreased Bacteroides compared to non-responders. A random forests classifier containing 11 microbial genera predicted CBT response with high accuracy (AUROC 0.96). Following treatment, CBT responders demonstrated reduced functional connectivity in regions of the sensorimotor, brainstem, salience, and default mode networks and changes in white matter in the basal ganglia and other structures. Brain changes correlated with microbiome shifts including Bacteroides expansion in responders. Conclusions Pre-treatment intestinal microbiota and serotonin levels were associated with CBT response, suggesting that peripheral signals from the microbiota can modulate central processes affected by CBT that generate abdominal symptoms in IBS. CBT response is characterized by co-correlated shifts in brain networks and gut microbiome that may reflect top-down effects of the brain on the microbiome during CBT. Video abstractJonathan P. JacobsArpana GuptaRavi R. BhattJacob BrawerKan GaoKirsten TillischVenu LagishettyRebecca FirthGregory D. GudleskiBenjamin M. EllingsonJennifer S. LabusBruce D. NaliboffJeffrey M. LacknerEmeran A. MayerBMCarticleCognitive behavioral therapyIrritable bowel syndromeBrain-gut-microbiome axisNeuroimagingBiomarkersOutcome predictionMicrobial ecologyQR100-130ENMicrobiome, Vol 9, Iss 1, Pp 1-14 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Cognitive behavioral therapy Irritable bowel syndrome Brain-gut-microbiome axis Neuroimaging Biomarkers Outcome prediction Microbial ecology QR100-130
spellingShingle	Cognitive behavioral therapy Irritable bowel syndrome Brain-gut-microbiome axis Neuroimaging Biomarkers Outcome prediction Microbial ecology QR100-130 Jonathan P. Jacobs Arpana Gupta Ravi R. Bhatt Jacob Brawer Kan Gao Kirsten Tillisch Venu Lagishetty Rebecca Firth Gregory D. Gudleski Benjamin M. Ellingson Jennifer S. Labus Bruce D. Naliboff Jeffrey M. Lackner Emeran A. Mayer Cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement
description	Abstract Background There is growing recognition that bidirectional signaling between the digestive tract and the brain contributes to irritable bowel syndrome (IBS). We recently showed in a large randomized controlled trial that cognitive behavioral therapy (CBT) reduces IBS symptom severity. This study investigated whether baseline brain and gut microbiome parameters predict CBT response and whether response is associated with changes in the brain-gut-microbiome (BGM) axis. Methods Eighty-four Rome III-diagnosed IBS patients receiving CBT were drawn from the Irritable Bowel Syndrome Outcome Study (IBSOS; ClinicalTrials.gov NCT00738920) for multimodal brain imaging and psychological assessments at baseline and after study completion. Fecal samples were collected at baseline and post-treatment from 34 CBT recipients for 16S rRNA gene sequencing, untargeted metabolomics, and measurement of short-chain fatty acids. Clinical measures, brain functional connectivity and microstructure, and microbiome features associated with CBT response were identified by multivariate linear and negative binomial models. Results At baseline, CBT responders had increased fecal serotonin levels, and increased Clostridiales and decreased Bacteroides compared to non-responders. A random forests classifier containing 11 microbial genera predicted CBT response with high accuracy (AUROC 0.96). Following treatment, CBT responders demonstrated reduced functional connectivity in regions of the sensorimotor, brainstem, salience, and default mode networks and changes in white matter in the basal ganglia and other structures. Brain changes correlated with microbiome shifts including Bacteroides expansion in responders. Conclusions Pre-treatment intestinal microbiota and serotonin levels were associated with CBT response, suggesting that peripheral signals from the microbiota can modulate central processes affected by CBT that generate abdominal symptoms in IBS. CBT response is characterized by co-correlated shifts in brain networks and gut microbiome that may reflect top-down effects of the brain on the microbiome during CBT. Video abstract
format	article
author	Jonathan P. Jacobs Arpana Gupta Ravi R. Bhatt Jacob Brawer Kan Gao Kirsten Tillisch Venu Lagishetty Rebecca Firth Gregory D. Gudleski Benjamin M. Ellingson Jennifer S. Labus Bruce D. Naliboff Jeffrey M. Lackner Emeran A. Mayer
author_facet	Jonathan P. Jacobs Arpana Gupta Ravi R. Bhatt Jacob Brawer Kan Gao Kirsten Tillisch Venu Lagishetty Rebecca Firth Gregory D. Gudleski Benjamin M. Ellingson Jennifer S. Labus Bruce D. Naliboff Jeffrey M. Lackner Emeran A. Mayer
author_sort	Jonathan P. Jacobs
title	Cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement
title_short	Cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement
title_full	Cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement
title_fullStr	Cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement
title_full_unstemmed	Cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement
title_sort	cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement
publisher	BMC
publishDate	2021
url	https://doaj.org/article/9211767c78c54222a359b868989af16a
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Cognitive behavioral therapy for irritable bowel syndrome induces bidirectional alterations in the brain-gut-microbiome axis associated with gastrointestinal symptom improvement

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