Neural correlates of perceived and relative resilience in male and female patients with irritable bowel syndrome.
functional magnetic resonance imaging
irritable bowel syndrome
psychological resilience
sex differences
Journal
Neurogastroenterology and motility
ISSN: 1365-2982
Titre abrégé: Neurogastroenterol Motil
Pays: England
ID NLM: 9432572
Informations de publication
Date de publication:
29 Nov 2023
29 Nov 2023
Historique:
revised:
22
09
2023
received:
22
06
2023
accepted:
09
10
2023
medline:
30
11
2023
pubmed:
30
11
2023
entrez:
30
11
2023
Statut:
aheadofprint
Résumé
Patients with irritable bowel syndrome (IBS) show lower resilience than healthy controls (HCs), associated with greater symptom severity and worse quality of life. However, little is known about affected markers of resilience or the influence of sex. Furthermore, as resilience is complex, a comprehensive assessment, with multiple resilience measures, is needed. Therefore, we aimed to evaluate perceived and relative resilience and their neural correlates in men and women with IBS. In 402 individuals (232 IBS [73.3% women] and 170 HCs [61.2% women]), perceived resilience was assessed by the Connor-Davidson Resilience Scale (CDRISC) and Brief Resilience Scale (BRS); relative resilience was assessed by the standardized residual of the Short Form-12 mental component summary score predicted by the Adverse Childhood Experiences score. Non-rotated partial least squares analysis of region-to-region resting-state connectivity data was used to define resilience-related signatures in HCs. Disease and sex-related differences within these signatures were investigated. Scores on all resilience measures were lower in IBS than in HCs (p's < 0.05). In all three resilience-related signatures, patients with IBS showed reduced connectivity largely involving the central autonomic network (p's < 0.001). Men with IBS showed lower CDRISC scores than women with IBS, and greater reductions in CDRISC-related connectivity, associated with worse symptom severity (p < 0.05). Individuals with IBS show reduced perceived and relative resilience, with reduced connectivity suggesting impaired homeostasis maintenance. Men with IBS may show additional impairment in specific aspects of resilience. Treatments aimed at improving resilience may benefit patients with IBS, especially men with IBS.
Sections du résumé
BACKGROUND
BACKGROUND
Patients with irritable bowel syndrome (IBS) show lower resilience than healthy controls (HCs), associated with greater symptom severity and worse quality of life. However, little is known about affected markers of resilience or the influence of sex. Furthermore, as resilience is complex, a comprehensive assessment, with multiple resilience measures, is needed. Therefore, we aimed to evaluate perceived and relative resilience and their neural correlates in men and women with IBS.
METHODS
METHODS
In 402 individuals (232 IBS [73.3% women] and 170 HCs [61.2% women]), perceived resilience was assessed by the Connor-Davidson Resilience Scale (CDRISC) and Brief Resilience Scale (BRS); relative resilience was assessed by the standardized residual of the Short Form-12 mental component summary score predicted by the Adverse Childhood Experiences score. Non-rotated partial least squares analysis of region-to-region resting-state connectivity data was used to define resilience-related signatures in HCs. Disease and sex-related differences within these signatures were investigated.
KEY RESULTS
RESULTS
Scores on all resilience measures were lower in IBS than in HCs (p's < 0.05). In all three resilience-related signatures, patients with IBS showed reduced connectivity largely involving the central autonomic network (p's < 0.001). Men with IBS showed lower CDRISC scores than women with IBS, and greater reductions in CDRISC-related connectivity, associated with worse symptom severity (p < 0.05).
CONCLUSIONS AND INFERENCES
CONCLUSIONS
Individuals with IBS show reduced perceived and relative resilience, with reduced connectivity suggesting impaired homeostasis maintenance. Men with IBS may show additional impairment in specific aspects of resilience. Treatments aimed at improving resilience may benefit patients with IBS, especially men with IBS.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e14710Subventions
Organisme : NIH HHS
Pays : United States
Informations de copyright
© 2023 The Authors. Neurogastroenterology & Motility published by John Wiley & Sons Ltd.
Références
Drossman DA. Functional gastrointestinal disorders: history, pathophysiology, clinical features and Rome IV. Gastroenterology. 2016;150:1262-1279.
Lacy BE, Mearin F, Lacy BE, Chang L, et al. Bowel disorders. Gastroenterology. 2016;150(6):1393-1407.
Park SH, Naliboff BD, Shih W, et al. Resilience is decreased in irritable bowel syndrome and associated with symptoms and cortisol response. Neurogastroenterol Motil. 2018;30(1):e13155.
Parker CH, Naliboff BD, Shih W, et al. The role of resilience in irritable bowel syndrome, other chronic gastrointestinal conditions, and the general population. Clin Gastroenterol Hepatol. 2021;19(12):2541-2550.
Ben-Ezra M, Hamama-Raz Y, Palgi S, Palgi Y. Cognitive appraisal and psychological distress among patients with irritable bowel syndrome. Isr J Psychiatry Relat Sci. 2015;52(1):54-59.
Mayer EA, Labus JS, Tillisch K, Cole SW, Baldi P. Towards a systems view of IBS. Nat Rev Gastroenterol Hepatol. 2015;12(10):592-605.
Hodes GE, Epperson CN. Sex differences in vulnerability and resilience to stress across the life span. Biol Psychiatry. 2019;86(6):421-432.
Franke HA. Toxic stress: effects, prevention and treatment. Children (Basel). 2014;1(3):390-402.
Kent M, Mardian AS, Regalado-Hustead ML, et al. Adaptive homeostatic strategies of resilient intrinsic self-regulation in extremes (RISE): a randomized controlled trial of a novel behavioral treatment for chronic pain. Front Psychol. 2021;12:613341.
Obradovic J, Portilla XA, Ballard PJ. Biological sensitivity to family income: differential effects on early executive functioning. Child Dev. 2016;87(2):374-384.
Wu L, Zhang X, Wang J, et al. The associations of executive functions with resilience in early adulthood: a prospective longitudinal study. J Affect Disord. 2021;282:1048-1054.
Miller GE, Chen E, Armstrong CC, et al. Functional connectivity in central executive network protects youth against cardiometabolic risks linked with neighborhood violence. Proc Natl Acad Sci U S A. 2018;115(47):12063-12068.
de Wit S, Wierenga LM, Oranje B, et al. Brain development in adolescents at ultra-high risk for psychosis: longitudinal changes related to resilience. Neuroimage Clin. 2016;12:542-549.
Schweizer S, Walsh ND, Stretton J, Dunn VJ, Goodyer IM, Dalgleish T. Enhanced emotion regulation capacity and its neural substrates in those exposed to moderate childhood adversity. Soc Cogn Affect Neurosci. 2016;11(2):272-281.
Rodman AM, Jenness JL, Weissman DG, Pine DS, McLaughlin KA. Neurobiological markers of resilience to depression following childhood maltreatment: the role of neural circuits supporting the cognitive control of emotion. Biol Psychiatry. 2019;86(6):464-473.
Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN. Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron. 2008;59(6):1037-1050.
Carnevali L, Koenig J, Sgoifo A, Ottaviani C. Autonomic and brain morphological predictors of stress resilience. Front Neurosci. 2018;12:228.
Nishimi K, Choi KW, Cerutti J, Powers A, Bradley B, Dunn EC. Measures of adult psychological resilience following early-life adversity: how congruent are different measures? Psychol Med. 2021;51(15):2637-2646.
Connor KM, Davidson JR. Development of a new resilience scale: the Connor-Davidson resilience scale (CD-RISC). Depress Anxiety. 2003;18(2):76-82.
Smith BW, Dalen J, Wiggins K, Tooley E, Christopher P, Bernard J. The brief resilience scale: assessing the ability to bounce back. Int J Behav Med. 2008;15(3):194-200.
Ye Y, Wu C, Yang C. The difference between the Connor-Davidson resilience scale and the brief resilience scale when assessing resilience: confirmatory factor analysis and predictive effects. Glob Ment Health (Camb.). 2022;9:339-346.
Amerio A, Bertuccio P, Santi F, et al. Gender differences in COVID-19 lockdown impact on mental health of undergraduate students. Front Psych. 2021;12:813130.
Haahr-Pedersen I, Perera C, Hyland P, et al. Females have more complex patterns of childhood adversity: implications for mental, social, and emotional outcomes in adulthood. Eur J Psychotraumatol. 2020;11(1):1708618.
Goldfarb EV, Seo D, Sinha R. Sex differences in neural stress responses and correlation with subjective stress and stress regulation. Neurobiol Stress. 2019;11:100177.
Kilpatrick LA, Istrin JJ, Gupta A, et al. Sex commonalities and differences in the relationship between resilient personality and the intrinsic connectivity of the salience and default mode networks. Biol Psychol. 2015;112:107-115.
Kilpatrick LA, Tillisch K. Irritable bowel syndrome. In: Schenck-Gustafsson K, DeCola PR, Pfaff DW, Pisetsky DS, eds. Handbook of Clinical Gender Medicine. Switzerland; 2012.
Chang L, Heitkemper MM. Gender differences in irritable bowel syndrome. Gastroenterology. 2002;123(5):1686-1701.
Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC. Functional bowel disorders. Gastroenterology. 2006;130(5):1480-1491.
Turner-Bowker D, Hogue SJ. Short form 12 health survey (SF-12). In: Michalos AC, ed. Encyclopedia of Quality of Life and Well-Being Research. Springer Netherlands; 2014:5954-5957.
Felitti VJ, Anda RF, Nordenberg D, et al. Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The adverse childhood experiences (ACE) study. Am J Prev Med. 1998;14(4):245-258.
Snaith RP. The hospital anxiety and depression scale. Health Qual Life Outcomes. 2003;1:29.
Patrick DL, Drossman DA, Frederick IO, DiCesare J, Puder KL. Quality of life in persons with irritable bowel syndrome: development and validation of a new measure. Dig Dis Sci. 1998;43(2):400-411.
Spiegel B, Bolus R, Harris LA, et al. Measuring irritable bowel syndrome patient-reported outcomes with an abdominal pain numeric rating scale. Aliment Pharmacol Ther. 2009;30(11-12):1159-1170.
Esteban O, Birman D, Schaer M, Koyejo OO, Poldrack RA, Gorgolewski KJ. MRIQC: advancing the automatic prediction of image quality in MRI from unseen sites. PloS One. 2017;12(9):e0184661.
Esteban O, Markiewicz CJ, Blair RW, et al. fMRIPrep: a robust preprocessing pipeline for functional MRI. Nat Methods. 2019;16(1):111-116.
Pruim RHR, Mennes M, van Rooij D, Llera A, Buitelaar JK, Beckmann CF. ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage. 2015;112:267-277.
Destrieux C, Fischl B, Dale A, Halgren E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage. 2010;53(1):1-15.
McIntosh AR, Lobaugh NJ. Partial least squares analysis of neuroimaging data: applications and advances. Neuroimage. 2004;23(Suppl 1):S250-S263.
Krzywinski M, Schein J, Birol I, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639-1645.
Lackner JM, Jaccard J, Group IBSOSR. Factors associated with efficacy of cognitive behavior therapy vs education for patients with irritable bowel syndrome. Clin Gastroenterol Hepatol. 2019;17(8):1500-1508.
Gaylord SA, Palsson OS, Garland EL, et al. Mindfulness training reduces the severity of irritable bowel syndrome in women: results of a randomized controlled trial. Am J Gastroenterol. 2011;106(9):1678-1688.
Peter J, Fournier C, Keip B, et al. Intestinal microbiome in irritable bowel syndrome before and after gut-directed hypnotherapy. Int J Mol Sci. 2018;19(11):3619.
Gupta A, Mayer EA, Acosta JR, et al. Early adverse life events are associated with altered brain network architecture in a sex- dependent manner. Neurobiol Stress. 2017;7:16-26.
Lamotte G, Shouman K, Benarroch EE. Stress and central autonomic network. Auton Neurosci. 2021;235:102870.
Son SJ, Park B, Choi JW, et al. Psychological resilience enhances the orbitofrontal network in the elderly with mild cognitive impairment. Front Psych. 2019;10:615.
Reekie YL, Braesicke K, Man MS, Roberts AC. Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex. Proc Natl Acad Sci U S A. 2008;105(28):9787-9792.
Hirose S, Osada T, Ogawa A, et al. Lateral-medial dissociation in orbitofrontal cortex-hypothalamus connectivity. Front Hum Neurosci. 2016;10:244.
Price JL. Connections of orbital cortex. In: Zald D, Rauch S, eds. The Orbitofrontal Cortex. Oxford University Press; 2006.
Saper CB. The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu Rev Neurosci. 2002;25:433-469.
Critchley HD, Nagai Y, Gray MA, Mathias CJ. Dissecting axes of autonomic control in humans: insights from neuroimaging. Auton Neurosci. 2011;161(1-2):34-42.
Roeckner AR, Oliver KI, Lebois LAM, van Rooij SJH, Stevens JS. Neural contributors to trauma resilience: a review of longitudinal neuroimaging studies. Transl Psychiatry. 2021;11(1):508.
Dolcos S, Hu Y, Iordan AD, Moore M, Dolcos F. Optimism and the brain: trait optimism mediates the protective role of the orbitofrontal cortex gray matter volume against anxiety. Soc Cogn Affect Neurosci. 2016;11(2):263-271.
Beissner F, Meissner K, Bar KJ, Napadow V. The autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function. J Neurosci. 2013;33(25):10503-10511.
Buckner RL, Andrews-Hanna JR, Schacter DL. The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci. 2008;1124:1-38.
Kano M, Yoshizawa M, Kono K, et al. Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome. Sci Rep. 2019;9(1):7358.
Tillisch K, Mayer EA, Labus JS, Stains J, Chang L, Naliboff BD. Sex specific alterations in autonomic function among patients with irritable bowel syndrome. Gut. 2005;54(10):1396-1401.
Manabe N, Tanaka T, Hata J, Kusunoki H, Haruma K. Pathophysiology underlying irritable bowel syndrome--from the viewpoint of dysfunction of autonomic nervous system activity. J Smooth Muscle Res. 2009;45(1):15-23.
Fukudo S. Stress and visceral pain: focusing on irritable bowel syndrome. Pain. 2013;154 Suppl 1:S63-S70.
Menon V, Uddin LQ. Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct. 2010;214(5-6):655-667.
Nogueira R, Abolafia JM, Drugowitsch J, Balaguer-Ballester E, Sanchez-Vives MV, Moreno-Bote R. Lateral orbitofrontal cortex anticipates choices and integrates prior with current information. Nat Commun. 2017;8:14823.
Labus JS, Naliboff BN, Fallon J, et al. Sex differences in brain activity during aversive visceral stimulation and its expectation in patients with chronic abdominal pain: a network analysis. Neuroimage. 2008;41(3):1032-1043.
Campbell-Sills L, Forde DR, Stein MB. Demographic and childhood environmental predictors of resilience in a community sample. J Psychiatr Res. 2009;43(12):1007-1012.
Cullen MR, Baiocchi M, Eggleston K, Loftus P, Fuchs V. The weaker sex? Vulnerable men and women's resilience to socio-economic disadvantage. SSM Popul Health. 2016;2:512-524.
Lei X, Han Z, Chen C, Bai L, Xue G, Dong Q. Sex differences in fiber connection between the striatum and subcortical and cortical regions. Front Comput Neurosci. 2016;10:100.
Sheerin CM, Stratton KJ, Amstadter AB, Education Clinical Center Mirecc Workgroup T, McDonald SD. Exploring resilience models in a sample of combat-exposed military service members and veterans: a comparison and commentary. Eur J Psychotraumatol. 2018;9(1):1486121.
Amstadter AB, Moscati A, Oxon MA, Maes HH, Myers JM, Kendler KS. Personality, cognitive/psychological traits and psychiatric resilience: a multivariate twin study. Pers Individ Dif. 2016;91:74-79.
Denckla CA, Consedine NS, Spies G, et al. Associations between neurocognitive functioning and social and occupational resilience among South African women exposed to childhood trauma. Eur J Psychotraumatol. 2017;8(1):1394146.
Cahill S, Hager R, Chandola T. The validity of the residuals approach to measuring resilience to adverse childhood experiences. Child Adolesc Psychiatry Ment Health. 2022;16(1):18.
Chen Y, Huang CC, Yang M, Wang J. Relationship between adverse childhood experiences and resilience in college students in China. J Fam Violence. 2023;38(4):623-632.
Subramaniam M, Abdin E, Vaingankar JA, et al. Association of adverse childhood experiences with diabetes in adulthood: results of a cross-sectional epidemiological survey in Singapore. BMJ Open. 2021;11(3):e045167.
Rosenberg SD, Lu W, Mueser KT, Jankowski MK, Cournos F. Correlates of adverse childhood events among adults with schizophrenia spectrum disorders. Psychiatr Serv. 2007;58(2):245-253.
Bonomi AE, Cannon EA, Anderson ML, Rivara FP, Thompson RS. Association between self-reported health and physical and/or sexual abuse experienced before age 18. Child Abuse Negl. 2008;32(7):693-701.
Black CJ, Yiannakou Y, Houghton LA, Ford AC. Epidemiological, clinical, and psychological characteristics of individuals with self-reported irritable bowel syndrome based on the Rome IV vs Rome III criteria. Clin Gastroenterol Hepatol. 2020;18(2):392-398.