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• Clinical Article •
Analysis of characteristics of brain functional network in Crohn's disease patients with chronic abdominal pain based on rs-fMRI graph theory
WU Xinyan  YANG Ling  YU Li  TANG Kaiqiang  ZHANG Lingqin  LIU Nian  LI Kang 

Cite this article as: WU X Y, YANG L, YU L, et al. Analysis of characteristics of brain functional network in Crohn's disease patients with chronic abdominal pain based on rs-fMRI graph theory[J]. Chin J Magn Reson Imaging, 2025, 16(4): 12-18, 113 DOI:10.12015/issn.1674-8034.2025.04.003.


[Abstract] Objective To explore the characteristic changes in the topological properties of the chronic pain-related neural network in patients with Crohn's disease (CD) using resting-state functional magnetic resonance imaging (rs-fMRI) combined with graph theory analysis.Materials and Methods A total of 20 chronic abdominal pain CD patients (APCD), 24 abdominal pain-free CD patients (FAPCD), and 30 healthy controls (HC) were included. Rs-fMRI and 3D-T1 data were collected from all subjects, and relevant clinical scale scores and clinical indicators were recorded. The topological indices of the functional network were compared among the three groups, and the correlations between the differences in brain regions and clinical scale scores were analyzed.Results Regarding global metrics, the FAPCD group exhibited lower small-worldness and normalized clustering coefficients compared to the APCD group (P < 0.05); however, neither the APCD group nor the FAPCD group showed significant differences when compared to the HC group (P > 0.05). Regarding nodal metrics, compared with the HC group, the degree centrality (DC) in the right anterior cingulate and paracingulate gyrus was significantly increased in the APCD group (P < 0.05). The DC and nodal efficiency (NE) in the left superior occipital gyrus and right postcentral gyrus were significantly decreased in the FAPCD group compared with the HC group (P < 0.05). Compared with the FAPCD group, the NE in the orbitofrontal region and the DC in the left precentral gyrus were lower in the APCD group (P < 0.05). Additionally, in APCD and FAPCD two combined CD groups, the increase in the visual analogue scale score for pain was associated with an increase in the DC of the left precentral gyrus (r = 0.386, P < 0.05).Conclusions The brain network topology characteristics of CD patients with chronic abdominal pain have changed, especially in DC and NE in specific brain regions. These changes may provide new directions for pain management and further research into the underlying neural mechanisms.
[Keywords] crohn's disease；abdominal pain；graph theory；brain network；resting-state functional magnetic resonance imaging；brain-gut axis

WU Xinyan1   YANG Ling2, 3   YU Li2, 3   TANG Kaiqiang2, 3   ZHANG Lingqin2, 3   LIU Nian1   LI Kang1, 2, 3*  

1 Department of Radiology, Affiliated Hospital of North Sichuan Medical College, Nanchong 637000, China

2 Department of Radiology, Chongqing General Hospital, Chongqing University, Chongqing, 401147, China

3 Department of Radiology, Chongqing General Hospital, Chongqing, 401147, China

Corresponding author: LI K, E-mail: lkrmyydoctor@126.com

Conflicts of interest   None.

Received  2025-01-17
Accepted  2025-04-10
DOI: 10.12015/issn.1674-8034.2025.04.003
Cite this article as: WU X Y, YANG L, YU L, et al. Analysis of characteristics of brain functional network in Crohn's disease patients with chronic abdominal pain based on rs-fMRI graph theory[J]. Chin J Magn Reson Imaging, 2025, 16(4): 12-18, 113 DOI:10.12015/issn.1674-8034.2025.04.003.

[1]
TORRES J, MEHANDRU S, COLOMBEL J F, et al. Crohn's disease[J]. Lancet, 2017, 389(10080): 1741-1755. DOI: 10.1016/S0140-6736(16)31711-1.
[2]
KING J A, UNDERWOOD F E, PANACCIONE N, et al. Trends in hospitalisation rates for inflammatory bowel disease in western versus newly industrialised countries: a population-based study of countries in the Organisation for Economic co-operation and Development[J]. 2019, 4(4): 287-295. DOI: 10.1016/S2468-1253(19)30013-5.
[3]
NG S C, SHI H Y, HAMIDI N, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies[J]. Lancet, 2017, 390(10114): 2769-2778. DOI: 10.1016/S0140-6736(17)32448-0.
[4]
SINOPOULOU V, GORDON M, AKOBENG A K, et al. Interventions for the management of abdominal pain in Crohn's disease and inflammatory bowel disease[J/OL]. 2021, 11(11): CD013531 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/34844288/. DOI: 10.1002/14651858.CD013531.pub2.
[5]
DREWES A M, OLESEN A E, FARMER A D, et al. Gastrointestinal pain[J/OL]. Nat Rev Dis Primers, 2020, 6(1): 1 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/31907359/. DOI: 10.1038/s41572-019-0135-7.
[6]
YARGER E, SANDBERG K. Updates in diagnosis and management of chronic abdominal pain[J/OL]. Curr Probl Pediatr Adolesc Health Care, 2020, 50(8): 100840 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/32859509/. DOI: 10.1016/j.cppeds.2020.100840.
[7]
BAILLIE S, NORTON C, SAXENA S, et al. Chronic abdominal pain in inflammatory bowel disease: a practical guide[J]. Frontline Gastroenterol, 2023, 15(2): 144-153. DOI: 10.1136/flgastro-2023-102471.
[8]
REGEV S, SCHWARTZ D, SARID O, et al. Randomised clinical trial: Psychological intervention improves work productivity and daily activity by reducing abdominal pain and fatigue in Crohn's disease[J]. Aliment Pharmacol Ther, 2023, 57(8): 861-871. DOI: 10.1111/apt.17399.
[9]
ABAUTRET-DALY Á, DEMPSEY E, PARRA-BLANCO A, et al. Gut-brain actions underlying comorbid anxiety and depression associated with inflammatory bowel disease[J]. Acta Neuropsychiatr, 2018, 30(5): 275-296. DOI: 10.1017/neu.2017.3.
[10]
KOUNTOURAS J, POLYZOS S A, DERETZI G. Multiple bidirectionality brain-gut interactions in patients with inflammatory bowel disease[J]. Gastroenterology, 2018, 155(5): 1651-1652. DOI: 10.1053/j.gastro.2018.06.091.
[11]
YANG L, HE P P, ZHANG L Q, et al. Altered resting-state brain functional activities and networks in Crohn's disease: a systematic review[J/OL]. Front Neurosci, 2024, 18: 1319359 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/38332859/. DOI: 10.3389/fnins.2024.1319359.
[12]
KONG N, ZHOU F N, ZHANG F, et al. Morphological and regional spontaneous functional aberrations in the brain associated with Crohn's disease: a systematic review and coordinate-based meta-analyses[J/OL]. Cereb Cortex, 2024, 34(4): bhae116 [2024-12-02]. https://academic.oup.com/cercor/article/doi/10.1093/cercor/bhae116/7639055. DOI: 10.1093/cercor/bhae116.
[13]
ÖHLMANN H, LANTERS L R, THEYSOHN N, et al. Distinct alterations in central pain processing of visceral and somatic pain in quiescent ulcerative colitis compared to irritable bowel syndrome and health[J]. J Crohns Colitis, 2023, 17(10): 1639-1651. DOI: 10.1093/ecco-jcc/jjad080.
[14]
BHATT R R, GUPTA A, LABUS J S, et al. Altered brain structure and functional connectivity and its relation to pain perception in girls with irritable bowel syndrome[J]. Psychosom Med, 2019, 81(2): 146-154. DOI: 10.1097/PSY.0000000000000655.
[15]
BAO C H, LIU P, LIU H R, et al. Difference in regional neural fluctuations and functional connectivity in Crohn's disease: a resting-state functional MRI study[J]. Brain Imaging Behav, 2018, 12(6): 1795-1803. DOI: 10.1007/s11682-018-9850-z.
[16]
PRÜß M S, BAYER A, BAYER K E, et al. Functional brain changes due to chronic abdominal pain in inflammatory bowel disease: A case-control magnetic resonance imaging study[J/OL]. Clin Transl Gastroenterol, 2022, 13(2): e00453 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/35060939/. DOI: 10.14309/ctg.0000000000000453.
[17]
GREGORICH M, SIMPSON S L, HEINZE G. Flexible parametrization of graph-theoretical features from individual-specific networks for prediction[J]. Stat Med, 2024, 43(13): 2592-2606. DOI: 10.1002/sim.10091.
[18]
VOLZ M S, FARMER A, SIEGMUND B. Reduction of chronic abdominal pain in patients with inflammatory bowel disease through transcranial direct current stimulation: a randomized controlled trial[J]. Pain, 2016, 157(2): 429-437. DOI: 10.1097/j.pain.0000000000000386.
[19]
LUKIC S, MIJAC D, FILIPOVIC B, et al. Chronic abdominal pain: gastroenterologist approach[J]. Dig Dis, 2022, 40(2): 181-186. DOI: 10.1159/000516977.
[20]
GOMOLLÓN F, DIGNASS A, ANNESE V, et al. 3rd European evidence-based consensus on the diagnosis and management of Crohn's disease 2016: part 1: diagnosis and medical management[J]. J Crohns Colitis, 2017, 11(1): 3-25. DOI: 10.1093/ecco-jcc/jjw168.
[21]
WANG J R, TAO A, ANDERSON W S, et al. Mesoscopic physiological interactions in the human brain reveal small-world properties[J/OL]. Cell Rep, 2021, 36(8): 109585 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/34433053/. DOI: 10.1016/j.celrep.2021.109585.
[22]
PAN W X, ZHAO F F, HAN B, et al. Emergence of brain-inspired small-world spiking neural network through neuroevolution[J/OL]. iScience, 2024, 27(2): 108845 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/38327781/. DOI: 10.1016/j.isci.2024.108845.
[23]
GARCÍA R A, MARTÍ A C, CABEZA C, et al. Small-worldness favours network inference in synthetic neural networks[J/OL]. Sci Rep, 2020, 10(1): 2296 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/32042036/. DOI: 10.1038/s41598-020-59198-7.
[24]
LIU P, LI R, BAO C H, et al. Altered topological patterns of brain functional networks in Crohn's disease[J]. Brain Imaging Behav, 2018, 12(5): 1466-1478. DOI: 10.1007/s11682-017-9814-8.
[25]
BIJSTERBOSCH J D, BECKMANN C F, WOOLRICH M W, et al. The relationship between spatial configuration and functional connectivity of brain regions revisited[J/OL]. eLife, 2019, 8: e44890 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/31066676/. DOI: 10.7554/eLife.44890.
[26]
YANG H J, WU H M, LI X H, et al. Functional disruptions of the brain network in low back pain: a graph-theoretical study[J]. Neuroradiology, 2023, 65(10): 1483-1495. DOI: 10.1007/s00234-023-03209-7.
[27]
CHEN R B, ZHONG M Y, ZHONG Y L. Abnormal topological organization of human brain connectome in primary dysmenorrhea patients using graph theoretical analysis[J]. J Pain Res, 2024, 17: 2789-2799. DOI: 10.2147/JPR.S470194.
[28]
XIN H T, YANG B N, JIA Y L, et al. Graph metrics reveal brain network topological property in neuropathic pain patients: A systematic review[J]. J Pain Res, 2024, 17: 3277-3286. DOI: 10.2147/JPR.S483466.
[29]
SABOURIN C J, MERRIKHI Y, LOMBER S G. Do blind people hear better?[J]. Trends Cogn Sci, 2022, 26(11): 999-1012. DOI: 10.1016/j.tics.2022.08.016.
[30]
KROPF E, SYAN S K, MINUZZI L, et al. From anatomy to function: the role of the somatosensory cortex in emotional regulation[J]. Braz J Psychiatry, 2019, 41(3): 261-269. DOI: 10.1590/1516-4446-2018-0183.
[31]
LI Z Y, MA Q, DENG Y T, et al. Irritable bowel syndrome is associated with brain health by neuroimaging, behavioral, biochemical, and genetic analyses[J]. Biol Psychiatry, 2024, 95(12): 1122-1132. DOI: 10.1016/j.biopsych.2023.12.024.
[32]
SHIRVALKAR P, PROSKY J, CHIN G, et al. First-in-human prediction of chronic pain state using intracranial neural biomarkers[J]. Nat Neurosci, 2023, 26(6): 1090-1099. DOI: 10.1038/s41593-023-01338-z.
[33]
ZHANG Y P, HONG G H, ZHANG C Y. Brain network changes in lumbar disc herniation induced chronic nerve roots compression syndromes[J/OL]. Neural Plast, 2022, 2022: 7912410 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/35607420/. DOI: 10.1155/2022/7912410.
[34]
DUAN S J, LIU L, LI G Y, et al. Altered functional connectivity within and between salience and sensorimotor networks in patients with functional constipation[J/OL]. Front Neurosci, 2021, 15: 628880 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/33776637/. DOI: 10.3389/fnins.2021.628880.
[35]
TAIT C, SAYUK G S. The brain-gut-microbiotal axis: a framework for understanding functional GI illness and their therapeutic interventions[J]. Eur J Intern Med, 2021, 84: 1-9. DOI: 10.1016/j.ejim.2020.12.023.
[36]
WANG L, LUO X Y, QING X L, et al. Symptom effects and central mechanism of acupuncture in patients with functional gastrointestinal disorders: a systematic review based on fMRI studies[J/OL]. BMC Gastroenterol, 2024, 24(1): 47 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/38267863/. DOI: 10.1186/s12876-024-03124-y.
[37]
ZHANG B L, JUNG M, TU Y H, et al. Identifying brain regions associated with the neuropathology of chronic low back pain: a resting-state amplitude of low-frequency fluctuation study[J/OL]. Br J Anaesth, 2019, 123(2): e303-e311 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/30948036/. DOI: 10.1016/j.bja.2019.02.021.
[38]
YU W J, WU X Y, CHEN Y N, et al. Pelvic pain alters functional connectivity between anterior cingulate cortex and hippocampus in both humans and a rat model[J/OL]. Front Syst Neurosci, 2021, 15: 642349 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/34149369/. DOI: 10.3389/fnsys.2021.642349.
[39]
SHUAI Y B, WANG B H, ZHANG X M, et al. Aberrant intrinsic brain activities in functional gastrointestinal disorders revealed by seed-based d mapping with permutation of subject images[J/OL]. Front Neurosci, 2024, 18: 1452216 [2024-10-25]. https://pubmed.ncbi.nlm.nih.gov/39618709/. DOI: 10.3389/fnins.2024.1452216.

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