Editorial: challenging established perceptions of brain–gut interactions in functional gastrointestinal disorders – brain–gut, gut–brain, or both?

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(1)This is a repository copy of Editorial: challenging established perceptions of brain–gut interactions in functional gastrointestinal disorders – brain–gut, gut–brain, or both?. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/107275/ Version: Accepted Version Article: Gracie, DJ and Ford, AC orcid.org/0000-0001-6371-4359 (2016) Editorial: challenging established perceptions of brain–gut interactions in functional gastrointestinal disorders – brain–gut, gut–brain, or both? Alimentary Pharmacology and Therapeutics, 44 (8). pp. 899-900. ISSN 0269-2813 https://doi.org/10.1111/apt.13762 (c) 2016, Wiley. This is the peer reviewed version of the following article:Gracie, DJ and Ford, AC (2016) Editorial: challenging established perceptions of brain–gut interactions in functional gastrointestinal disorders – brain–gut, gut–brain, or both? Alimentary Pharmacology and Therapeutics, 44 (8). pp. 899-900 which has been published in final form at https://doi.org/10.1111/apt.13762. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving. Reuse Unless indicated otherwise, fulltext items are protected by copyright with all rights reserved. The copyright exception in section 29 of the Copyright, Designs and Patents Act 1988 allows the making of a single copy solely for the purpose of non-commercial research or private study within the limits of fair dealing. The publisher or other rights-holder may allow further reproduction and re-use of this version - refer to the White Rose Research Online record for this item. Where records identify the publisher as the copyright holder, users can verify any specific terms of use on the publisher’s website. Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing eprints@whiterose.ac.uk including the URL of the record and the reason for the withdrawal request. eprints@whiterose.ac.uk https://eprints.whiterose.ac.uk/

(2) Accepted 21st July 2016 TITLE PAGE Title: Challenging established perceptions of brain-gut interactions in functional gastrointestinal disorders: brain-gut, gut-brain, or both? Short “running” title: FGIDs: brain-gut, gut-brain or both? Authors: David J. Gracie1, 2 , Alexander C. Ford1, 2 1 Leeds Gastroenterology Institute, St. James’s University Hospital, Leeds, UK. 2 Leeds Institute of Biomedical and Clinical Sciences, University of Leeds, Leeds, UK. Abbreviations: Correspondence: CI confidence interval FD functional dyspepsia FGID functional gastrointestinal disorder HADS hospital anxiety and depression scale IBS irritable bowel syndrome OR odds ratio Dr. David J. Gracie Leeds Gastroenterology Institute Room 125 4th Floor Bexley Wing

(3) St. James’s University Hospital Beckett Street Leeds United Kingdom LS9 7TF Keywords: Email: djgracie1982@doctors.org.uk Telephone: +447980765615 Facsimile: +441132429722 irritable bowel syndrome functional dyspepsia depression anxiety Word count: 517

(4) Irritable bowel syndrome (IBS) and functional dyspepsia (FD) are functional gastrointestinal disorders (FGID) of uncertain cause. Observational studies demonstrate a high prevalence of psychological co-morbidity in FGIDs, 1-5 supporting the hypothesis that the development of these conditions is centrally mediated, via brain-gut interactions. Despite this, emerging evidence also suggests that functional bowel symptoms occurring de novo are associated with the development of anxiety or depression, implying gut-brain interactions may also exist. 6, 7 Koloski et al. attempted to delineate the relationship between brain and gut in FGIDs in a random population sample of 2885 Australian adults. 8 At inclusion, and after a follow- up interval of 12 months, participants completed the Rome III questionnaire for IBS and FD, and the hospital anxiety and depression scale (HADS) questionnaire to assess for psychological distress. In total, 1900 (67.6%) participants completed both baseline and 12month follow-up questionnaires. Individuals without IBS or FD, but with anxiety or depression at study entry, who went on to develop either IBS or FD subsequently were classed as having brain-gut interactions. Those with IBS or FD, but without anxiety or depression at inclusion, and who subsequently developed anxiety or depression were labelled as having gut-brain interactions. The study demonstrated an increased odds of developing both IBS and FD with increasing anxiety severity (odds ratio (OR) per standard deviation increase in baseline HADS anxiety score = 1.31; 95% confidence interval (CI) 1.06-1.61, P = 0.01 and OR = 1.28; 95% CI 1.05-1.55, P = 0.01, respectively). There was also an increased odds of developing both IBS and FD in those with increasing depression severity (OR per standard deviation increase in baseline HADS depression score = 1.54; 95% CI 1.29-1.83, P <0.001 and OR = 1.55; 95% CI 1.32-1.83, P <0.001, respectively).

(5) Among those with IBS, but without psychological distress at baseline, there was an increase in mean anxiety and depression scores at 12 months (mean difference in anxiety score = 0.34; 95% CI 0.13-0.55, P = 0.002 and mean difference in depression score = 0.81; 95% CI 0.47-1.15, P <0.001). A similar effect was also noted in those with pre-existing FD (mean difference in anxiety score = 0.38; 95% CI 0.14-0.63, P = 0.002 and mean difference in depression score = 0.92; 95% CI 0.57-1.27, P <0.001). This study highlights the interplay between brain and gut and suggests that, in FGIDs, these interactions are likely to be bi-directional. Although this assertion in itself is not novel, 6 the limited follow-up of only 12 months suggests the role of brain-gut interactions is more influential and important than previously described. However, a causal link between anxiety and depression, and the development of FGIDs during longitudinal follow-up, may not be universal. Indeed, the findings of this study are in conflict with those published by the same investigators in a Scandinavian cohort of patients where anxiety, but not depression, was associated with the development of FD. 9 Although these data support the existence of a bidirectional relationship between psychological co-morbidities and FGIDs, inconsistencies in the apparent influence of psychological distress on the development, and evolution, of functional symptoms requires further longitudinal investigation.

(6) AUTHORSHIP Guarantor of the article: DJ Gracie Author contributions: DJG and ACF drafted the manuscript. Both authors commented on drafts of the paper. Both authors have approved the final draft of the article. ACKNOWLEDGEMENTS Declaration of personal interests: None. Declaration of funding interests: None.

(7) REFERENCES 1. Sayuk GS, Elwing JE, Lustman PJ, Clouse RE. High somatic symptom burdens and functional gastrointestinal disorders. Clin Gastroenterol Hepatol 2007;5(5):556-62. 2. Aro P, Talley NJ, Ronkainen J, et al. Anxiety is associated with uninvestigated and functional dyspepsia (Rome III criteria) in a Swedish population-based study. Gastroenterology 2009;137(1):94-100. 3. Wouters MM, Van Wanrooy S, Nguyen A, et al. Psychological comorbidity increases the risk for postinfectious IBS partly by enhanced susceptibility to develop infectious gastroenteritis. Gut 2016;65(8):1279-88. 4. Patel P, Bercik P, Morgan DG, et al. Irritable bowel syndrome is significantly associated with somatisation in 840 patients, which may drive bloating. Aliment Pharmacol Ther 2015;41(5):449-58. 5. Gracie DJ, Bercik P, Morgan DG, et al. No increase in prevalence of somatization in functional vs organic dyspepsia: a cross-sectional survey. Neurogastroenterol Motil 2015;27(7):1024-31. 6. Koloski NA, Jones M, Kalantar J, Weltman M, Zaguirre J, Talley NJ. The brain--gut pathway in functional gastrointestinal disorders is bidirectional: a 12-year prospective population-based study. Gut 2012;61(9):1284-90. 7. Liebregts T, Adam B, Bredack C, et al. Immune activation in patients with irritable bowel syndrome. Gastroenterology 2007;132(3):913-20. 8. Koloski NA, Jones M, Talley NJ. Evidence that independent gut-to-brain and brain- to-gut pathways operate in the irritable bowel syndrome and functional dyspepsia: A 1-year population-based prospective study. Aliment Pharmacol Ther 2016 (in press).

(8) 9. Aro P, Talley NJ, Johansson SE, Agreus L, Ronkainen J. Anxiety Is Linked to New- Onset Dyspepsia in the Swedish Population: A 10-Year Follow-up Study. Gastroenterology 2015;148(5):928-37.

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