Distinct Alterations in Central Pain Processing of Visceral and Somatic Pain in Quiescent Ulcerative Colitis Compared to Irritable Bowel Syndrome and Health.


Journal

Journal of Crohn's & colitis
ISSN: 1876-4479
Titre abrégé: J Crohns Colitis
Pays: England
ID NLM: 101318676

Informations de publication

Date de publication:
08 Nov 2023
Historique:
medline: 13 11 2023
pubmed: 10 5 2023
entrez: 10 5 2023
Statut: ppublish

Résumé

Despite relevance to pain chronicity, disease burden, and treatment, mechanisms of pain perception for different types of acute pain remain incompletely understood in patients with inflammatory bowel disease [IBD]. Building on experimental research across pain modalities, we herein addressed behavioural and neural correlates of visceral versus somatic pain processing in women with quiescent ulcerative colitis [UC] compared to irritable bowel syndrome [IBS] as a patient control group and healthy women [HC]. Thresholds for visceral and somatic pain were assessed with rectal distensions and cutaneous thermal pain, respectively. Using functional magnetic resonance imaging, neural and behavioural responses to individually calibrated and intensity-matched painful stimuli from both modalities were compared. Pain thresholds were comparable across groups, but visceral thresholds correlated with gastrointestinal symptom severity and chronic stress burden exclusively within UC. Upon experience of visceral and somatic pain, both control groups demonstrated enhanced visceral pain-induced neural activation and greater perceived pain intensity, whereas UC patients failed to differentiate between pain modalities at both behavioural and neural levels. When confronted with acute pain from multiple bodily sites, UC patients' responses are distinctly altered. Their failure to prioritise pain arising from the viscera may reflect a lack of adaptive behavioural flexibility, possibly resulting from long-lasting central effects of repeated intestinal inflammatory insults persisting during remission. The role of psychological factors, particularly chronic stress, in visceral sensitivity and disease-specific alterations in the response to acute pain call for dedicated mechanistic research as a basis for tailoring interventions for intestinal and extraintestinal pain symptoms in IBD.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
Despite relevance to pain chronicity, disease burden, and treatment, mechanisms of pain perception for different types of acute pain remain incompletely understood in patients with inflammatory bowel disease [IBD]. Building on experimental research across pain modalities, we herein addressed behavioural and neural correlates of visceral versus somatic pain processing in women with quiescent ulcerative colitis [UC] compared to irritable bowel syndrome [IBS] as a patient control group and healthy women [HC].
METHODS METHODS
Thresholds for visceral and somatic pain were assessed with rectal distensions and cutaneous thermal pain, respectively. Using functional magnetic resonance imaging, neural and behavioural responses to individually calibrated and intensity-matched painful stimuli from both modalities were compared.
RESULTS RESULTS
Pain thresholds were comparable across groups, but visceral thresholds correlated with gastrointestinal symptom severity and chronic stress burden exclusively within UC. Upon experience of visceral and somatic pain, both control groups demonstrated enhanced visceral pain-induced neural activation and greater perceived pain intensity, whereas UC patients failed to differentiate between pain modalities at both behavioural and neural levels.
CONCLUSIONS CONCLUSIONS
When confronted with acute pain from multiple bodily sites, UC patients' responses are distinctly altered. Their failure to prioritise pain arising from the viscera may reflect a lack of adaptive behavioural flexibility, possibly resulting from long-lasting central effects of repeated intestinal inflammatory insults persisting during remission. The role of psychological factors, particularly chronic stress, in visceral sensitivity and disease-specific alterations in the response to acute pain call for dedicated mechanistic research as a basis for tailoring interventions for intestinal and extraintestinal pain symptoms in IBD.

Identifiants

pubmed: 37161902
pii: 7158889
doi: 10.1093/ecco-jcc/jjad080
pmc: PMC10637045
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1639-1651

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : 316803389-SFB 1280

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of European Crohn’s and Colitis Organisation.

Références

Psychoneuroendocrinology. 2018 Dec;98:101-107
pubmed: 30125791
Brain Behav Immun. 2021 Feb;92:211-222
pubmed: 33249172
Anesthesiology. 2018 Jun;128(6):1241-1254
pubmed: 29494401
Inflamm Bowel Dis. 2009 Dec;15(12):1851-8
pubmed: 19462421
Clin Gastroenterol Hepatol. 2017 Oct;15(10):1500-1503
pubmed: 28392439
Neurogastroenterol Motil. 2021 Mar;33(3):e13998
pubmed: 33034406
Brain Behav Immun. 2019 Aug;80:616-632
pubmed: 31063848
World J Gastroenterol. 2011 Jun 14;17(22):2723-33
pubmed: 21734780
Brain Behav Immun. 2023 Feb;108:328-339
pubmed: 36535608
BMC Med Res Methodol. 2012 Apr 01;12:42
pubmed: 22463771
Pain. 2022 Mar 1;163(3):538-547
pubmed: 34224497
Psychophysiology. 2020 Feb;57(2):e13474
pubmed: 31529522
J Pain Symptom Manage. 1999 Sep;18(3):180-7
pubmed: 10517039
Crohns Colitis 360. 2021 Jun 23;3(3):otab041
pubmed: 36776657
Brain Behav Immun. 2011 Oct;25(7):1333-41
pubmed: 21536124
Lancet Gastroenterol Hepatol. 2020 Dec;5(12):1053-1062
pubmed: 33010814
J Clin Med. 2021 Jan 20;10(3):
pubmed: 33498197
Pain. 2002 Jun;97(3):235-246
pubmed: 12044620
Neurogastroenterol Motil. 2017 Oct;29(10):1-10
pubmed: 28560758
Neuroimage. 2016 Apr 15;130:104-114
pubmed: 26854560
Am J Physiol Gastrointest Liver Physiol. 2012 Jul 15;303(2):G141-54
pubmed: 22595988
Gut. 2015 Mar;64(3):418-27
pubmed: 24833636
Pain. 2005 Jun;115(3):398-409
pubmed: 15911167
Pain. 2019 Aug;160(8):1719-1728
pubmed: 31335642
Gastroenterology. 1987 Oct;93(4):727-33
pubmed: 3623019
Neurogastroenterol Motil. 2021 Jun;33(6):e14078
pubmed: 33368950
Neuroimage Clin. 2021;30:102613
pubmed: 33823388
J Behav Med. 2013 Oct;36(5):477-87
pubmed: 22752251
Inflamm Bowel Dis. 2022 Mar 30;28(4):599-610
pubmed: 34734248
Inflamm Bowel Dis. 2013 Oct;19(11):2380-6
pubmed: 23942564
Acta Psychiatr Scand. 1983 Jun;67(6):361-70
pubmed: 6880820
Neuroimage. 2003 Jul;19(3):1233-9
pubmed: 12880848
Ann N Y Acad Sci. 2012 Jul;1262:108-17
pubmed: 22823442
Nat Rev Dis Primers. 2016 Mar 24;2:16014
pubmed: 27159638
Inflamm Bowel Dis. 2021 Oct 18;27(10):1576-1584
pubmed: 33382065
Front Psychiatry. 2020 Apr 30;11:286
pubmed: 32425821
Inflamm Bowel Dis. 2011 Aug;17(8):1769-77
pubmed: 21744432
Cereb Cortex. 2011 Jul;21(7):1498-506
pubmed: 21097516
Physiol Rev. 2018 Jan 1;98(1):477-504
pubmed: 29351513
Dtsch Arztebl Int. 2020 Aug 17;117(33-34):564-574
pubmed: 33148393
World J Gastroenterol. 2010 Jul 7;16(25):3168-77
pubmed: 20593502
Gut. 2019 Sep;68(9):1701-1715
pubmed: 31175206
PLoS One. 2016 Jun 22;11(6):e0156666
pubmed: 27332879
Crohns Colitis 360. 2021 Aug 26;3(3):otab061
pubmed: 36776665
J Pediatr Gastroenterol Nutr. 2016 Nov;63(5):500-507
pubmed: 27574880
Psychoneuroendocrinology. 2020 Jan;111:104501
pubmed: 31715444
Gastroenterology. 2002 Apr;122(4):1140-56
pubmed: 11910364
Mol Pain. 2019 Jan-Dec;15:1744806919891327
pubmed: 31709891
Scand J Gastroenterol. 2011 Jul;46(7-8):981-7
pubmed: 21623672
Lancet Gastroenterol Hepatol. 2019 Aug;4(8):632-642
pubmed: 31122802
Front Neurol. 2021 Oct 20;12:733035
pubmed: 34744973
J Clin Med. 2022 Jul 22;11(15):
pubmed: 35893357
Psychosom Med. 2018 Nov/Dec;80(9):826-835
pubmed: 29870435
Pain. 2017 Aug;158(8):1599-1608
pubmed: 28426553
Inflamm Bowel Dis. 2023 Mar 1;29(3):405-416
pubmed: 35590449
Gut. 2005 Oct;54(10):1481-91
pubmed: 16162953
Therap Adv Gastroenterol. 2016 Mar;9(2):199-212
pubmed: 26929782
Commun Biol. 2021 May 11;4(1):553
pubmed: 33976383
Nat Commun. 2020 Nov 23;11(1):5939
pubmed: 33230131
Gastroenterology. 2022 Oct;163(4):995-1023.e3
pubmed: 35716771
Am J Physiol Gastrointest Liver Physiol. 2019 Jun 1;316(6):G692-G700
pubmed: 30735453
Neurogastroenterol Motil. 2016 Sep;28(9):1419-32
pubmed: 27132547
Neuroimage Clin. 2019;21:101602
pubmed: 30472166
Mol Psychiatry. 2022 Mar;27(3):1792-1804
pubmed: 35046525
Clin Transl Gastroenterol. 2017 Jan 19;8(1):e214
pubmed: 28102860
BMJ. 1989 Jan 14;298(6666):82-6
pubmed: 2563951
Eur J Pain. 2014 Apr;18(4):567-74
pubmed: 24027228
Neuroscience. 2005;133(2):533-42
pubmed: 15896917
Am J Gastroenterol. 2008 Jan;103(1):162-9
pubmed: 17916108
Gastroenterology. 2016 Feb 18;:
pubmed: 27144627
Nat Rev Gastroenterol Hepatol. 2016 Sep 26;13(10):613-21
pubmed: 27667579
J Neurophysiol. 2003 Jun;89(6):3294-303
pubmed: 12611986
Gastroenterol Hepatol (N Y). 2011 Apr;7(4):235-41
pubmed: 21857821
J Neuroimmunol. 2002 May;126(1-2):116-25
pubmed: 12020963

Auteurs

Hanna Öhlmann (H)

Department of Medical Psychology and Medical Sociology, Ruhr University Bochum, Bochum, Germany.

Laura Ricarda Lanters (LR)

Department of Neurology, Center for Translational Neuro- and Behavioral Sciences, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.

Nina Theysohn (N)

Institute of Diagnostic and Interventional Radiology and Neuroradiology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.

Jost Langhorst (J)

Department for Internal and Integrative Medicine, Sozialstiftung Bamberg, Bamberg, Germany.
Department for Integrative Medicine, Medical Faculty, University of Duisburg-Essen, Essen, Germany.

Harald Engler (H)

Institute of Medical Psychology and Behavioral Immunobiology, Center for Translational Neuro- and Behavioral Sciences, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.

Adriane Icenhour (A)

Department of Medical Psychology and Medical Sociology, Ruhr University Bochum, Bochum, Germany.

Sigrid Elsenbruch (S)

Department of Medical Psychology and Medical Sociology, Ruhr University Bochum, Bochum, Germany.
Department of Neurology, Center for Translational Neuro- and Behavioral Sciences, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH