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. 2021 Nov 29;11(12):1580.
doi: 10.3390/brainsci11121580.

Altered Structural Covariance of Insula, Cerebellum and Prefrontal Cortex Is Associated with Somatic Symptom Levels in Irritable Bowel Syndrome (IBS)

Cecilia Grinsvall  1   2   3 , Lukas Van Oudenhove  4   5   6 , Patrick Dupont  5   7 , Hyo Jin Ryu  8 , Maria Ljungberg  9   10 , Jennifer S Labus  11 , Hans Törnblom  1 , Emeran A Mayer  11 , Magnus Simrén  1   12
Affiliations

Altered Structural Covariance of Insula, Cerebellum and Prefrontal Cortex Is Associated with Somatic Symptom Levels in Irritable Bowel Syndrome (IBS)

Cecilia Grinsvall et al. Brain Sci. .

Abstract

Somatization, defined as the presence of multiple somatic symptoms, frequently occurs in irritable bowel syndrome (IBS) and may constitute the clinical manifestation of a neurobiological sensitization process. Brain imaging data was acquired with T1 weighted 3 tesla MRI, and gray matter morphometry were analyzed using FreeSurfer. We investigated differences in networks of structural covariance, based on graph analysis, between regional gray matter volumes in IBS-related brain regions between IBS patients with high and low somatization levels, and compared them to healthy controls (HCs). When comparing IBS low somatization (N = 31), IBS high somatization (N = 35), and HCs (N = 31), we found: (1) higher centrality and neighbourhood connectivity of prefrontal cortex subregions in IBS high somatization compared to healthy controls; (2) higher centrality of left cerebellum in IBS low somatization compared to both IBS high somatization and healthy controls; (3) higher centrality of the anterior insula in healthy controls compared to both IBS groups, and in IBS low compared to IBS high somatization. The altered structural covariance of prefrontal cortex and anterior insula in IBS high somatization implicates that prefrontal processes may be more important than insular in the neurobiological sensitization process associated with IBS high somatization.

Keywords: brain imaging; brain morphometry; central sensitization; irritable bowel syndrome; somatization; structural covariance.

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Conflict of interest statement

C.G. nothing to declare. L.V.O. has received an unrestricted research grant from Nestlé (not related to the present work), and serves as a consultant for Danone. P.D. nothing to declare. J.S.L. nothing to declare. H.J.R. nothing to declare. M.L. nothing to declare. H.T. has served as Consultant/Advisory Board member for Almirall and Allergan as a speaker for Tillotts, Takeda, Shire and Almirall. E.A.M. is a member of Scientific Advisory Boards for Danone, Viome, Amare, Prolacta, Axial Biotherapeutics, Whole Biome, Ubiome, Bloom Bioscience and Mahana Therapeutics. M.S. received unrestricted research grants from Danone, Glycom and Ferring Pharmaceuticals, and served as a Consultant/Advisory Board member for AstraZeneca, Danone, Nestlé, Almirall, Allergan, Albireo, Glycom, and Shire, and as a speaker for Tillotts, Menarini, Takeda, Shire, Allergan, Biocodex, Alimentary Health, AlfaSigma and Almirall.

Figures

Figure 1
Figure 1
Histogram of the PHQ-14 results in the IBS cohort.
Figure 2
Figure 2
Differences in covariance between groups, significant at p < 0.001. (a) Differences in covariance between IBS high and low somatization. Covariance greater in IBS high somatization compared to IBS low somatization are shown with red lines, and covariance greater in IBS low somatization compared to IBS high somatization are shown with blue lines. (b) Differences in covariance between healthy controls and IBS low somatization. Covariance greater in healthy controls compared to IBS low somatization are shown with red lines, and covariance greater in IBS low somatization compared to healthy controls are shown with blue lines. (c) Differences in covariance between healthy controls and IBS high somatization. Covariance greater in healthy controls compared to IBS high somatization are shown with red lines, and covariance greater in IBS high somatization compared to healthy controls are shown with blue lines.
Figure 2
Figure 2
Differences in covariance between groups, significant at p < 0.001. (a) Differences in covariance between IBS high and low somatization. Covariance greater in IBS high somatization compared to IBS low somatization are shown with red lines, and covariance greater in IBS low somatization compared to IBS high somatization are shown with blue lines. (b) Differences in covariance between healthy controls and IBS low somatization. Covariance greater in healthy controls compared to IBS low somatization are shown with red lines, and covariance greater in IBS low somatization compared to healthy controls are shown with blue lines. (c) Differences in covariance between healthy controls and IBS high somatization. Covariance greater in healthy controls compared to IBS high somatization are shown with red lines, and covariance greater in IBS high somatization compared to healthy controls are shown with blue lines.
Figure 3
Figure 3
Regions with maximal hub scores in the different groups. Regions belonging to the prefrontal cortex are shown in blue and insular regions are shown in red. (a) Regions with maximal hub scores in IBS high somatization. Frontal view of the brain, with the left of the figure being the right of the brain, showing regions with the maximum hub score in IBS high somatization: left and right triangular part of the inferior frontal gyrus, right superior frontal gyrus and right orbital gyri. (b) Regions with maximal hub scores in IBS low somatization. Axial view of the brain, with the left of the figure being the right of the brain, showing regions with the maximum hub score in IBS low somatization: right triangular part of the inferior frontal gyrus and left short insular gyri.
Figure 4
Figure 4
Regions with maximal hub scores in healthy controls: Axial view of the brain, with the left of the figure being the right of the brain, showing regions with the maximum hub score in HCs: left and right short insular gyri and left superior segment of the circular sulcus of the insula.
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