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Research progress in MRI of microbiota‐gut‐brain axis dysbiosis
LIU Wanting  ZHANG Xiaoling 

Cite this article as: LIU W T, ZHANG X L. Research progress in MRI of microbiota‐gut‐brain axis dysbiosis[J]. Chin J Magn Reson Imaging, 2023, 14(2): 158-162. DOI:10.12015/issn.1674-8034.2023.02.028.


[Abstract] The gut‐brain axis is a bidirectional information communication pathway. As one of the key regulators of the gut‐brain axis, the gut microbiota is not only involved in maintaining intestinal homeostasis and regulating intestinal function, but also can directly communicate and transmit information with the brain through the complex enteric nervous system. At present, studies have confirmed that the dysbiosis of intestinal microbiota may be related to neurodegenerative diseases, mental and metabolic diseases, but the mechanism behind it has not been clearly elucidated. Focusing on the role and research progress of magnetic resonance imaging technology in dysbiosis of intestinal microbiota and neurodegenerative disorders, psychosocial and metabolic diseases, this paper summarizes the correlation between intestinal microflora and brain structure and function, aiming to explore the action mechanism of intestinal microbes in diseases and provide theoretical support in clinical treatment.
[Keywords] gut microbial communities;gut-brain axis;magnetic resonance imaging;functional magnetic resonance imaging;multimodal magnetic resonance imaging

LIU Wanting1   ZHANG Xiaoling2*  

1 Graduate School of Xi'an Medical University, Xi'an 710068, China

2 MRI Room of Shaanxi Provincial People's Hospital, Xi'an 710068, China

*Correspondence to: Zhang XL, E-mail: zxl.822@163.com

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 82170820); Key Research and Development Plan of Shaanxi (No. 2018ZDXM-SF-038).
Received  2022-09-15
Accepted  2023-02-08
DOI: 10.12015/issn.1674-8034.2023.02.028
Cite this article as: LIU W T, ZHANG X L. Research progress in MRI of microbiota‐gut‐brain axis dysbiosis[J]. Chin J Magn Reson Imaging, 2023, 14(2): 158-162. DOI:10.12015/issn.1674-8034.2023.02.028.

[1]
ZHENG D, LIWINSKI T, ELINAV E. Interaction between microbiota and immunity in health and disease[J]. Cell Res, 2020, 30(6): 492-506. DOI: 10.1038/s41422-020-0332-7.
[2]
DABKE K, HENDRICK G, DEVKOTA S. The gut microbiome and metabolic syndrome[J]. J Clin Invest, 2019, 129(10): 4050-4057. DOI: 10.1172/JCI129194.
[3]
COOK T M, MANSUY-AUBERT V. Communication between the gut microbiota and peripheral nervous system in health and chronic disease[J/OL]. Gut Microbes, 2022, 14(1): 2068365 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/35482894/. DOI: 10.1080/19490976.2022.2068365.
[4]
BRUCE-KELLER A J, SALBAUM J M, BERTHOUD H R. Harnessing Gut Microbes for Mental Health: Getting From Here to There[J]. Biol Psychiatry, 2018, 83(3): 214-223. DOI: 10.1016/j.biopsych.2017.08.014.
[5]
AGUSTI A, GARCIA-PARDO M P, LOPEZ-ALMELA I, et al. Interplay Between the Gut-Brain Axis, Obesity and Cognitive Function[J/OL]. Front Neurosci, 2018, 12: 155 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/29615850/. DOI: 10.3389/fnins.2018.00155.
[6]
BONAZ B, BAZIN T, PELLISSIER S. The Vagus Nerve at the Interface of the Microbiota-Gut-Brain Axis[J/OL]. Front Neurosci, 2018, 12: 49 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/29467611/. DOI: 10.3389/fnins.2018.00049.
[7]
WANG J J, ZHANG R G, DONG X R. Recent advance in interaction between intestinal flora and brain function[J]. Chin J Neuromed, 2018, 17(12): 1281-1286. DOI: 10.3760/cma.j.issn.1671-8925.2018.12.000.
[8]
DE VADDER F, GRASSET E, MANNERAS HOLM L, et al. Gut microbiota regulates maturation of the adult enteric nervous system via enteric serotonin networks[J]. Proc Natl Acad Sci U S A, 2018, 115(25): 6458-6463. DOI: 10.1073/pnas.1720017115.
[9]
SHUKLA R, GHOSHAL U, RANJAN P, et al. Expression of Toll-like Receptors, Pro-, and Anti-inflammatory Cytokines in Relation to Gut Microbiota in Irritable Bowel Syndrome: The Evidence for Its Micro-organic Basis[J]. J Neurogastroenterol Motil, 2018, 24(4): 628-642. DOI: 10.5056/jnm18130.
[10]
ABDEL-HAQ R, SCHLACHETZKI J C M, GLASS C K, et al. Microbiome-microglia connections via the gut-brain axis[J]. J Exp Med, 2019, 216(1): 41-59. DOI: 10.1084/jem.20180794.
[11]
MORAIS L H, SCHREIBER H L T, MAZMANIAN S K. The gut microbiota-brain axis in behaviour and brain disorders[J]. Nat Rev Microbiol, 2021, 19(4): 241-255. DOI: 10.1038/s41579-020-00460-0.
[12]
LIU S, ZHANG X, HUANG G M, et al. Investigate the whole level alteration of dynamic functional connectivity of attention network in patients with major depressive disorder based on magnetic resonance imaging[J]. Chin J Magn Reson Imaging, 2022, 13(6): 40-44. DOI: 10.12015/issn.1674-8034.2022.06.008.
[13]
WANG X T, DONG X X, LI S Y. Identification of Alzheimer's disease and mild cognitive impairment patients using individual-specific functional connectivity[J]. Chin J Magn Reson Imaging, 2022, 13(4): 56-61, 68. DOI: 10.12015/issn.1674-8034.2022.04.010.
[14]
WEN X, CHEN J, LIAO C X, et al. Study on time variability of brain activity in patients with irritable bowel syndrome with diarrhea based on dynamic amplitude of low-frequency fluctuation[J]. Chin J Magn Reson Imaging, 2022, 13(6): 61-65. DOI: 10.12015/issn.1674-8034.2022.06.012.
[15]
ZHANG P, WU G W, YU F X, et al. Abnormal Regional Neural Activity and Reorganized Neural Network in Obesity: Evidence from Resting-State fMRI[J]. Obesity (Silver Spring), 2020, 28(7): 1283-1291. DOI: 10.1002/oby.22839.
[16]
BIALECKA-DEBEK A, GRANDA D, Szmidt M K, et al. Gut Microbiota, Probiotic Interventions, and Cognitive Function in the Elderly: A Review of Current Knowledge[J/OL]. Nutrients, 2021, 13(8): 2514 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/34444674/. DOI: 10.3390/nu13082514.
[17]
MARGOLIS K G, CRYAN J F, MAYER E A. The Microbiota-Gut-Brain Axis: From Motility to Mood[J]. Gastroenterology, 2021, 160(5): 1486-1501. DOI: 10.1053/j.gastro.2020.10.066.
[18]
GUPTA A, OSADCHIY V, MAYER E A. Brain-gut-microbiome interactions in obesity and food addiction[J]. Nat Rev Gastroenterol Hepatol, 2020, 17(11): 655-672. DOI: 10.1038/s41575-020-0341-5.
[19]
WU L, HAN Y, ZHENG Z, et al. Altered Gut Microbial Metabolites in Amnestic Mild Cognitive Impairment and Alzheimer's Disease: Signals in Host-Microbe Interplay[J/OL]. Nutrients, 2021, 13(1): 228 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/33466861/. DOI: 10.3390/nu13010228.
[20]
LIU P, JIA X Z, CHEN Y, et al. Gut microbiota interacts with intrinsic brain activity of patients with amnestic mild cognitive impairment[J]. CNS Neurosci Ther, 2021, 27(2): 163-173. DOI: 10.1111/cns.13451.
[21]
SCHMAHMANN J D. The cerebellum and cognition[J]. Neurosci Lett, 2019, 688: 62-75. DOI: 10.1016/j.neulet.2018.07.005.
[22]
WANAPAISAN P, CHUANSANGEAM M, NOPNIPA S, et al. Association between Gut Microbiota with Mild Cognitive Impairment and Alzheimer's Disease in a Thai Population[J]. Neurodegener Dis, 2022, 22(2): 43-54. DOI: 10.1159/000526947.
[23]
LIANG X, FU Y, CAO W T, et al. Gut microbiome, cognitive function and brain structure: a multi-omics integration analysis[J/OL]. Transl Neurodegener, 2022, 11(1): 49 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/36376937/. DOI: 10.1186/s40035-022-00323-z.
[24]
VERHAAR B J H, HENDRIKSEN H M A, DE LEEUW F A, et al. Gut Microbiota Composition Is Related to AD Pathology[J/OL]. Front Immunol, 2021, 12: 794519 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/35173707/. DOI: 10.3389/fimmu.2021.794519.
[25]
NHO K, KUEIDER-PAISLEY A, MAHMOUDIANDEHKORDI S, et al. Altered bile acid profile in mild cognitive impairment and Alzheimer's disease: Relationship to neuroimaging and CSF biomarkers[J]. Alzheimers Dement, 2019, 15(2): 232-244. DOI: 10.1016/j.jalz.2018.08.012.
[26]
ASAOKA D, XIAO J, TAKEDA T, et al. Effect of Probiotic Bifidobacterium breve in Improving Cognitive Function and Preventing Brain Atrophy in Older Patients with Suspected Mild Cognitive Impairment: Results of a 24-Week Randomized, Double-Blind, Placebo-Controlled Trial[J]. J Alzheimers Dis, 2022, 88(1): 75-95. DOI: 10.3233/JAD-220148.
[27]
HIRAYAMA M, OHNO K. Parkinson's Disease and Gut Microbiota[J]. Ann Nutr Metab, 2021, 77(Suppl 2): 28-35. DOI: 10.1159/000518147.
[28]
SINDERMANN L, REDLICH R, OPEL N, et al. Systematic transdiagnostic review of magnetic-resonance imaging results: Depression, anxiety disorders and their co-occurrence[J]. J Psychiatr Res, 2021, 142: 226-239. DOI: 10.1016/j.jpsychires.2021.07.022.
[29]
HUANG X, LI L, LING Z, et al. Gut microbiome diversity mediates the association between right dorsolateral prefrontal cortex and anxiety level[J]. Brain Imaging Behav, 2022, 16(1): 397-405. DOI: 10.1007/s11682-021-00513-9.
[30]
STRANDWITZ P, KIM K H, TEREKHOVA D, et al. GABA-modulating bacteria of the human gut microbiota[J]. Nat Microbiol, 2019, 4(3): 396-403. DOI: 10.1038/s41564-018-0307-3.
[31]
COLEY E J L, MAYER E A, OSADCHIY V, et al. Early life adversity predicts brain-gut alterations associated with increased stress and mood[J/OL]. Neurobiol Stress, 2021, 15: 100348 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/34113697/. DOI: 10.1016/j.ynstr.2021.100348.
[32]
TILLISCH K, MAYER E A, GUPTA A, et al. Brain Structure and Response to Emotional Stimuli as Related to Gut Microbial Profiles in Healthy Women[J]. Psychosom Med, 2017, 79(8): 905-913. DOI: 10.1097/PSY.0000000000000493.
[33]
MA X, ASIF H, DAI L, et al. Alteration of the gut microbiome in first-episode drug-naive and chronic medicated schizophrenia correlate with regional brain volumes[J]. J Psychiatr Res, 2020, 123: 136-144. DOI: 10.1016/j.jpsychires.2020.02.005.
[34]
OHTANI T, DEL R E E, LEVITT J J, et al. Progressive symptom-associated prefrontal volume loss occurs in first-episode schizophrenia but not in affective psychosis[J]. Brain Struct Funct, 2018, 223(6): 2879-2892. DOI: 10.1007/s00429-018-1634-0.
[35]
LI S, SONG J, KE P, et al. The gut microbiome is associated with brain structure and function in schizophrenia[J/OL]. Sci Rep, 2021, 11(1): 9743 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/33963227/. DOI: 10.1038/s41598-021-89166-8.
[36]
VAN RHEENEN T E, CROPLEY V, ZALESKY A, et al. Widespread Volumetric Reductions in Schizophrenia and Schizoaffective Patients Displaying Compromised Cognitive Abilities[J]. Schizophr Bull, 2018, 44(3): 560-574. DOI: 10.1093/schbul/sbx109.
[37]
PUNTIS S, MINICHINO A, DE CRESCENZO F, et al. Specialised early intervention teams (extended time) for recent-onset psychosis[J/OL]. Cochrane Database Syst Rev, 2020, 11(11): CD013287 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/33135812/. DOI: 10.1002/14651858.CD013287.pub2.
[38]
FORD A C, SPERBER A D, CORSETTI M, et al. Irritable bowel syndrome[J]. Lancet, 2020, 396(10263): 1675-1688. DOI: 10.1016/S0140-6736(20)31548-8.
[39]
ANCONA A, PETITO C, IAVARONE I, et al. The gut-brain axis in irritable bowel syndrome and inflammatory bowel disease[J]. Dig Liver Dis, 2021, 53(3): 298-305. DOI: 10.1016/j.dld.2020.11.026.
[40]
LABUS J S, HOLLISTER E B, JACOBS J, et al. Differences in gut microbial composition correlate with regional brain volumes in irritable bowel syndrome[J/OL]. Microbiome, 2017, 5(1): 49 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/28457228/. DOI: 10.1186/s40168-017-0260-z.
[41]
LABUS J S, OSADCHIY V, HSIAO E Y, et al. Evidence for an association of gut microbial Clostridia with brain functional connectivity and gastrointestinal sensorimotor function in patients with irritable bowel syndrome, based on tripartite network analysis[J/OL]. Microbiome, 2019, 7(1): 45 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/30898151/. DOI: 10.1186/s40168-019-0656-z.
[42]
OSADCHIY V, MAYER E A, GAO K, et al. Analysis of brain networks and fecal metabolites reveals brain-gut alterations in premenopausal females with irritable bowel syndrome[J/OL]. Transl Psychiatry, 2020, 10(1): 367 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/33139708/. DOI: 10.1038/s41398-020-01071-2.
[43]
IZUNO S, YOSHIHARA K, SUDO N. Role of Gut Microbiota in the Pathophysiology of Stress-Related Disorders: Evidence from Neuroimaging Studies[J]. Ann Nutr Metab, 2021, 77(Suppl 2): 4-10. DOI: 10.1159/000517420.
[44]
PINTO-SANCHEZ M I, HALL G B, GHAJAR K, et al. Probiotic Bifidobacterium longum NCC3001 Reduces Depression Scores and Alters Brain Activity: A Pilot Study in Patients With Irritable Bowel Syndrome[J/OL]. Gastroenterology, 2017, 153(2): 448-459 e448 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/28483500/. DOI: 10.1053/j.gastro.2017.05.003.
[45]
DONG T S, MAYER E A, OSADCHIY V, et al. A Distinct Brain-Gut-Microbiome Profile Exists for Females with Obesity and Food Addiction[J]. Obesity (Silver Spring), 2020, 28(8): 1477-1486. DOI: 10.1002/oby.22870.
[46]
DONG T S, GUAN M, MAYER E A, et al. Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain's reward center[J/OL]. Gut Microbes, 2022, 14(1): 2051999 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/35311453/. DOI: 10.1080/19490976.2022.2051999.
[47]
OSADCHIY V, LABUS J S, GUPTA A, et al. Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects[J/OL]. PLoS One, 2010.3390/nu1210292418, 13(8): e0201772 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/30080865/. DOI: 10.1371/journal.pone.0201772.
[48]
DONG T S, GUPTA A, JACOBS J P, et al. Improvement in Uncontrolled Eating Behavior after Laparoscopic Sleeve Gastrectomy Is Associated with Alterations in the Brain-Gut-Microbiome Axis in Obese Women[J/OL]. Nutrients, 2020, 12(10): 2924 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/32987837/. DOI: 10.3390/nu12102924.
[49]
HONG J, BO T, XI L, et al. Reversal of Functional Brain Activity Related to Gut Microbiome and Hormones After VSG Surgery in Patients With Obesity[J/OL]. J Clin Endocrinol Metab, 2021, 106(9): e3619-e3633 [2022-09-14]. https://pubmed.ncbi.nlm.nih.gov/33950216/. DOI: 10.1210/clinem/dgab297.

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