Irritable bowel syndrome in women: Association between decreased insular subregion volumes and gastrointestinal symptoms

Nawroz Barazanji; J Paul Hamilton; Adriane Icenhour; Rozalyn A Simon; Olga Bednarska; Sofie Tapper; Anders Tisell; Peter Lundberg; Maria Engström; Susanna Walter

doi:10.1016/j.nicl.2022.103128

Irritable bowel syndrome in women: Association between decreased insular subregion volumes and gastrointestinal symptoms

Neuroimage Clin. 2022:35:103128. doi: 10.1016/j.nicl.2022.103128. Epub 2022 Jul 28.

Authors

Affiliations

¹ Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection, Linköping University, Sweden; Department of Gastroenterology, Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden. Electronic address: Nawroz.Barazanji@liu.se.
² Center for Social and Affective Neuroscience, Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden; Center for Medical Image Science and Visualization (CMIV), Linköping University, Linköping, Sweden.
³ Department of Medical Psychology and Medical Sociology, Ruhr University Bochum, Bochum, Germany.
⁴ Center for Medical Image Science and Visualization (CMIV), Linköping University, Linköping, Sweden; Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden.
⁵ Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection, Linköping University, Sweden; Department of Gastroenterology, Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden.
⁶ Center for Medical Image Science and Visualization (CMIV), Linköping University, Linköping, Sweden; Department of Radiation Physics, and Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden.
⁷ Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection, Linköping University, Sweden; Department of Gastroenterology, Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden; Center for Medical Image Science and Visualization (CMIV), Linköping University, Linköping, Sweden; Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden.

Abstract

Objective: Irritable bowel syndrome (IBS) is a chronic pain disorder characterized by disturbed interactions between the gut and the brain with depression as a common comorbidity. In both IBS and depression, structural brain alterations of the insular cortices, key structures for pain processing and interoception, have been demonstrated but the specificity of these findings remains unclear. We compared the gray matter volume (GMV) of insular cortex (IC) subregions in IBS women and healthy controls (HC) and examined relations to gastrointestinal (GI) symptoms and glutamate + glutamine (Glx) concentrations. We further analyzed GMV of IC subregions in women with major depression (MDD) compared to HC and addressed possible differences between depression, IBS, IBS with depression and HC.

Design: Women with IBS (n = 75), MDD (n = 41) and their respective HC (n = 39 and n = 43) underwent structural brain MRI. IC subregion volumes were estimated using statistical parametric mapping software. General linear model approaches were applied to IC volumetric data and FDR-corrected partial correlation analyses assessed relations between GMV, GI symptoms and Glx concentrations.

Results: IBS patients had significantly smaller IC subregions than HC in both hemispheres but there was no significant difference between MDD compared with IBS and HC for any insular subregion. In IBS, the dorsal anterior insular volumes were negatively correlated with symptoms of nausea and pain, and the left ventral subregion showed a positive correlation with straining to defecate, while the posterior subregion volumes showed no relation to symptoms. In the anterior insula, concentration of Glx showed positive correlations with GMV bilaterally in HC and with GMV of the right anterior insula in IBS.

Conclusion: As the interoceptive cortex, the insula shows substantial and disease-specific structural differences in patients with chronic interoceptive visceral pain. Particularly changes in the anterior proportions might be related to chronic exposure to or enhanced salience towards adverse interoceptive visceral signals and could be linked to biochemical changes, calling for further multimodal and longitudinal work.

Keywords: Brain morphometry; Depression; Gray matter volume; Gut-brain axis; IBS symptoms; Insula.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Cerebral Cortex / diagnostic imaging
Female
Gray Matter / diagnostic imaging
Humans
Irritable Bowel Syndrome* / complications
Irritable Bowel Syndrome* / diagnostic imaging
Magnetic Resonance Imaging
Pain