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Deficient habituation to repeated rectal distensions in irritable bowel syndrome patients with visceral hypersensitivity
Linköping University, Department of Clinical and Experimental Medicine, Division of Neuro and Inflammation Science. Linköping University, Faculty of Medicine and Health Sciences.
Oppenheimer Center for Neurobiology of Stress, Division of Digestive Diseases, Department of Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA.
Oppenheimer Center for Neurobiology of Stress, Division of Digestive Diseases, Department of Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA.
Oppenheimer Center for Neurobiology of Stress, Division of Digestive Diseases, Department of Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA.
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2015 (English)In: Neurogastroenterology and Motility, ISSN 1350-1925, E-ISSN 1365-2982, Vol. 27, no 5, 646-655 p.Article in journal (Refereed) Published
Abstract [en]

Background Irritable bowel syndrome (IBS) patients show evidence of altered central processing of visceral signals. One of the proposed alterations in sensory processing is an altered engagement of endogenous pain modulation mechanisms. The aim was to test the hypothesis that IBS patients with (IBS-S) and without visceral hypersensitivity (IBS-N) differ in their ability to engage endogenous pain modulation mechanism during habituation to repeated visceral stimuli.

Methods Brain blood oxygen level dependent (BOLD) response was measured during repeated rectal distension and its anticipation in 33 IBS patients with and without visceral hypersensitivity and 18 healthy controls (HCs). BOLD response to early and late phase of the distension series was compared within and between groups.

Key Results While BOLD response was similar during the early phase of the experiment, IBS-S showed greater BOLD response than IBS-N and HCs during the late phase of the distension series. IBS-S showed increasing BOLD response both to the anticipation and delivery of low intensity rectal distensions in brain regions including insula, anterior and mid cingulate cortex. IBS-N showed decreasing BOLD response to repeated rectal distensions in brain regions including insula, prefrontal cortex and amygdala.

Conclusions & Inferences These findings are consistent with compromised ability of IBS-S to respond to repeated delivery of rectal stimuli, both in terms of sensitization of sensory pathways and habituation of emotional arousal. The fact that both IBS subgroups met Rome criteria, and did not differ in terms of reported symptom severity demonstrates that similar symptom patterns can result from different underlying neurobiological mechanisms.

Place, publisher, year, edition, pages
2015. Vol. 27, no 5, 646-655 p.
Keyword [en]
irritable bowel syndrome, brain-gut interaction, fMRI, visceral sensitivity
National Category
Gastroenterology and Hepatology Neurosciences
Identifiers
URN: urn:nbn:se:liu:diva-122143DOI: 10.1111/nmo.12537ISI: 000364742000007PubMedID: 25777251OAI: oai:DiVA.org:liu-122143DiVA: diva2:862044
Note

Funding agencies: County Council of Ostergotland, Sweden; National Institute of Health [DK 64531]

Available from: 2015-10-20 Created: 2015-10-20 Last updated: 2016-02-15Bibliographically approved
In thesis
1. Irritable Bowel Syndrome: Studies of central pathophysiological mechanisms and effects of treatment
Open this publication in new window or tab >>Irritable Bowel Syndrome: Studies of central pathophysiological mechanisms and effects of treatment
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Background and aims

Irritable bowel syndrome (IBS) is a common gastrointestinal disorder characterized by abdominal pain and altered bowel habits. The societal costs of the disorder are significant, as are its negative effects on quality of life. Medical treatment options are limited, but psychological treatments such as hypnotherapy have proven to be effective. Important pathophysiological mechanisms include disturbances in brain processing of visceral sensation and expectation of visceral sensation. Increased sensation of stimuli (hypersensitivity) is present in a subset of IBS patients to distensions in the lower part of the gastrointestinal tract, indicating a probable important pathophysiological mechanism in IBS. The overall aim of the thesis was to further study the central pathophysiological mechanisms involved in IBS. Specifically, we aimed to identify differences in brain response to standardized repeated rectal distensions and expectation of these stimuli between IBS patients (with or without perceptual rectal hypersensitivity), and healthy controls. Furthermore, we aimed to investigate IBS patients´ brain responses to standardized rectal distensions and expectation of these stimuli after either a successful course hypnotherapy or educational intervention.

Methods

Functional magnetic resonance imaging (fMRI) data were acquired and analyzed from 15 IBS patients with visceral hypersensitivity, and 18 IBS patients with normal visceral sensitivity (papers I and II). In paper III, fMRI data were analyzed from IBS patients who reported significant symptom reduction after either a course of hypnotherapy, or an educational intervention. FMRI data from IBS patients and healthy controls were also compared.

Results

The findings reported in papers I and II suggest, that the differences in brain response between IBS patients with and without rectal hypersensitivity, can be explained by changes in brain response during the course of the experiment. Even though the brain responses were similar between groups during the early phase of the experiment, they became substantially different during the late phase. The IBS patients with rectal hypersensitivity demonstrated increased brain response in several brain regions and networks involved in visceral sensation and processing. In contrast, IBS patients with normal rectal sensitivity exhibited reduced brain response during the late phase of the experiment. As reported in paper III, similar symptom reduction was achieved for both treatments. The symptomatic improvement was associated with a reduction of response in the anterior insula, indicating an attenuated awareness of the stimuli. The hypnotherapy group had a reduction of response in the posterior insula, indicating less input to the brain, possibly due to changed activity in endogenous pain modulatory systems. In patients who reported significant symptom reduction following treatment, the brain response to rectal distension got more similar to that observed in healthy controls.

Conclusions

The results from papers I and II indicate that a subpopulation of IBS patients lacks the ability to habituate to repeated rectal distensions and expectation of these stimuli. Results from paper III indicate that the abnormal processing of visceral stimuli in IBS can be altered, and that the treatments probably had a normalizing effect on the central processing abnormality of visceral signals in IBS.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2015. 62 p.
Series
Linköping University Medical Dissertations, ISSN 0345-0082 ; 1472
National Category
Neurology Radiology, Nuclear Medicine and Medical Imaging Gastroenterology and Hepatology
Identifiers
urn:nbn:se:liu:diva-122144 (URN)10.3384/diss.diva-122144 (DOI)978-91-7685-983-4 (print) (ISBN)
Public defence
2015-11-06, Berzeliussalen, Campus US, Linköping, 13:00 (English)
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Available from: 2015-10-20 Created: 2015-10-20 Last updated: 2016-04-24Bibliographically approved

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Lowén, Mats B. O.Lundberg, PeterThorell, Lars-HåkanStröm, MagnusEngström, MariaWalter, Susanna
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Division of Neuro and Inflammation ScienceFaculty of Medicine and Health SciencesCenter for Medical Image Science and Visualization (CMIV)Division of Radiological SciencesDepartment of Radiation PhysicsDepartment of Gastroentorology
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