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Advances in functional magnetic resonance in non-neuropsychiatric systemic lupus erythematosus
CHEN Jialing  AO Feng 

Cite this article as: CHEN J L, AO F. Advances in functional magnetic resonance in non-neuropsychiatric systemic lupus erythematosus[J]. Chin J Magn Reson Imaging, 2024, 15(10): 158-164. DOI:10.12015/issn.1674-8034.2024.10.027.


[Abstract] Non-neuropsychiatric systemic lupus erythematosus (non-NPSLE) is a subtype of systemic lupus erythematosus (SLE) disease that involves the central nervous system and continues to impair patients' health. The pathogenesis of non-NPSLE is still unclear. Functional magnetic resonance techniques can provide non-invasive and valuable research results, which can help to study the neurobiological mechanisms and biological markers of non-NPSLE from multiple levels and perspectives. In recent years, a variety of functional magnetic resonance techniques have been applied to non-NPSLE to explore its brain functional changes. In summary, this paper reviews the findings and potential shortcomings of functional magnetic resonance techniques in the application of non-NPSLE, aiming to provide a direction for future research on non-NPSLE.
[Keywords] lupus erythematosus, systemic;magnetic resonance imaging;blood oxygenation level dependent;diffusion tensor imaging;arterial spin labeling

CHEN Jialing1, 2, 3   AO Feng1, 2, 3*  

1 School of Biomedical Engineering Hubei University of Medicine, Shiyan 442000, China

2 Department of Radiological Imaging Center, Renmin Hospital, Hubei University of Medicine, Shiyan 442000, China

3 Institute of Radiological Imaging, Renmin Hospital, Hubei University of Medicine, Shiyan 442000, China

Corresponding author: AO F, E-mail: aofeng19841112@163.com

Conflicts of interest   None.

Received  2024-06-14
Accepted  2024-10-10
DOI: 10.12015/issn.1674-8034.2024.10.027
Cite this article as: CHEN J L, AO F. Advances in functional magnetic resonance in non-neuropsychiatric systemic lupus erythematosus[J]. Chin J Magn Reson Imaging, 2024, 15(10): 158-164. DOI:10.12015/issn.1674-8034.2024.10.027.

[1]
ARINGER M, JOHNSON S R. Classifying and diagnosing systemic lupus erythematosus in the 21st century[J/OL]. Rheumatology (Oxford), 2020, 59(Supplement_5): v4-v11 [2024-06-14]. https://doi.org/10.1093/rheumatology/keaa379. DOI: 10.1093/rheumatology/keaa379.
[2]
RAGHUNATH S, GLIKMANN-JOHNSTON Y, GOLDER V, et al. Clinical associations of cognitive dysfunction in systemic lupus erythematosus[J/OL]. Lupus Sci Med, 2023, 10(1): e000835 [2024-06-14]. https://doi.org/10.1136/lupus-2022-000835. DOI: 10.1136/lupus-2022-000835.
[3]
MAGRO-CHECA C, RAMIRO S, RÚA-FIGUEROA I, et al. Central nervous system involvement in systemic lupus erythematosus: Data from the Spanish Society of Rheumatology Lupus Register (RELESSER)[J/OL]. Semin Arthritis Rheum, 2023, 58: 152121 [2024-06-14]. https://doi.org/10.1016/j.semarthrit.2022.152121. DOI: 10.1016/j.semarthrit.2022.152121.
[4]
ACR AD HOC COMMITTEE ON NEUROPSYCHIATRIC LUPUS NOMENCLATURE. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes[J]. Arthritis Rheum, 1999, 42(4): 599-608. DOI: 10.1002/1529-0131(199904)42:4<599::AID-ANR2>3.0.CO;2-F.
[5]
LI X L, XIA J G. Advances in resting-state functional magnetic resonance imaging in systemic lupus erythematosus[J]. J Clin Radiol, 2022, 41(5): 970-973. DOI: 10.13437/j.cnki.jcr.2022.05.024.
[6]
SARWAR S, MOHAMED A S, ROGERS S, et al. Neuropsychiatric Systemic Lupus Erythematosus: A 2021 Update on Diagnosis, Management, and Current Challenges[J/OL]. Cureus, 2021 [2024-06-14]. https://www.cureus.com/articles/65863-neuropsychiatric-systemic-lupus-erythematosus-a-2021-update-on-diagnosis-management-and-current-challenges. DOI: 10.7759/cureus.17969.
[7]
ZHANG S, LI M, ZHANG L, et al. Clinical features and outcomes of neuropsychiatric systemic lupus erythematosus in China[J]. J Immunol Res, 2021, 2021: 1-10. DOI: 10.1155/2021/1349042.
[8]
MACKAY M, TANG C C. Advanced neuroimaging in neuropsychiatric systemic lupus erythematosus[J]. Curr Opin Neurol, 2020, 33(3): 353-361. DOI: 10.1097/WCO.0000000000000822.
[9]
CAO Z Y, WANG N, WU J T. Advances in functional brain imaging in systemic lupus erythematosus[J]. J Clin Radiol, 2020, 39(12): 2556-2559. DOI: 10.13437/j.cnki.jcr.2020.12.044.
[10]
LANGENSEE L, MÅRTENSSON J, JÖNSEN A, et al. Cognitive performance in systemic lupus erythematosus patients: a cross-sectional and longitudinal study[J/OL]. BMC Rheumatol, 2022, 6(1): 22 [2024-06-14]. https://doi.org/10.1186/s41927-022-00253-3. DOI: 10.1186/s41927-022-00253-3.
[11]
ZARFESHANI A, CARROLL K R, VOLPE B T, et al. Cognitive impairment in SLE: Mechanisms and therapeutic approaches[J/OL]. Curr Rheumatol Rep, 2021, 23(4): 25 [2024-06-14]. https://doi.org/10.1007/s11926-021-00992-1. DOI: 10.1007/s11926-021-00992-1.
[12]
RUBINSTEIN T, BRICKMAN A M, CHENG B, et al. Periodontitis and brain magnetic resonance imaging markers of Alzheimer's disease and cognitive aging[J]. Alzheimers Dement, 2024, 20(3): 2191-2208. DOI: 10.1002/alz.13683.
[13]
GÖLLER S, NICKEL K, HORSTER I, et al. State or trait: the neurobiology of anorexia nervosa-contributions of a functional magnetic resonance imaging study[J/OL]. J Eat Disord, 2022, 10(1): 77 [2024-06-14]. https://doi.org/10.1186/s40337-022-00598-7. DOI: 10.1186/s40337-022-00598-7.
[14]
SANTOS L A, SULLIVAN B, KVIST O, et al. Diffusion tensor imaging of the physis: the ABC's[J]. Pediatr Radiol, 2023, 53(12): 2355-2368. DOI: 10.1007/s00247-023-05753-z.
[15]
ZIMNY A, SZMYRKA-KACZMAREK M, SZEWCZYK P, et al. In vivo evaluation of brain damage in the course of systemic lupus erythematosus using magnetic resonance spectroscopy, perfusion-weighted and diffusion-tensor imaging[J]. Lupus, 2014, 23(1): 10-19. DOI: 10.1177/0961203313511556.
[16]
SHAPIRA-LICHTER I, WEINSTEIN M, LUSTGARTEN N, et al. Impaired diffusion tensor imaging findings in the corpus callosum and cingulum may underlie impaired learning and memory abilities in systemic lupus erythematosus[J]. Lupus, 2016, 25(11): 1200-1208. DOI: 10.1177/0961203316636471.
[17]
ZHAO L, TAN X, WANG J, et al. Brain white matter structural networks in patients with non-neuropsychiatric systemic lupus erythematosus[J]. Brain Imaging Behav, 2018, 12(1): 142-155. DOI: 10.1007/s11682-017-9681-3.
[18]
JANELLE F, IORIO-MORIN C, D'AMOUR S, et al. Superior longitudinal fasciculus: A review of the anatomical descriptions with functional correlates[J/OL]. Front Neurol, 2022, 13: 794618 [2024-06-14]. https://doi.org/10.3389/fneur.2022.794618. DOI: 10.3389/fneur.2022.794618.
[19]
XU M, TAN X, ZHANG X, et al. Alterations of white matter structural networks in patients with non-neuropsychiatric systemic lupus erythematosus identified by probabilistic tractography and connectivity-based analyses[J]. Neuroimage Clin, 2017, 13: 349-360. DOI: 10.1016/j.nicl.2016.12.021.
[20]
NYSTEDT J, NILSSON M, JÖNSEN A, et al. Altered white matter microstructure in lupus patients: a diffusion tensor imaging study[J/OL]. Arthritis Res Ther, 2018, 20(1): 21 [2024-06-14]. https://doi.org/10.1186/s13075-018-1516-0. DOI: 10.1186/s13075-018-1516-0.
[21]
XIA R, CHEN X, ENGEL T A, et al. Common and distinct neural mechanisms of attention[J]. Trends Cogn Sci, 2024, 28(6): 554-567. DOI: 10.1016/j.tics.2024.01.005.
[22]
RIBEIRO M, YORDANOVA Y N, NOBLET V, et al. White matter tracts and executive functions: a review of causal and correlation evidence[J]. Brain, 2024, 147(2): 352-371. DOI: 10.1093/brain/awad308.
[23]
YANG X, NIU W, WU K, et al. Diffusion kurtosis imaging‐based habitat analysis identifies high-risk molecular subtypes and heterogeneity matching in diffuse gliomas[J/OL]. Ann Clin Transl Neurol, 2024: acn3.52128 [2024-06-14]. https://doi.org/10.1002/acn3.52128. DOI: 10.1002/acn3.52128.
[24]
HENRIQUES R N, CORREIA M M, MARRALE M, et al. Diffusional kurtosis imaging in the diffusion imaging in python project[J/OL]. Front Hum Neurosci, 2021, 15: 675433 [2024-06-14]. https://doi.org/10.3389/fnhum.2021.675433. DOI: 10.3389/fnhum.2021.675433.
[25]
ZHANG Z, WANG Y, SHEN Z, et al. The neurochemical and microstructural changes in the brain of systemic lupus erythematosus patients: A multimodal MRI study[J/OL]. Sci Rep, 2016, 6(1): 19026 [2024-06-14]. https://doi.org/10.1038/srep19026. DOI: 10.1038/srep19026.
[26]
WANG X, HUANG L, GUO W, et al. Cerebral microstructural and microvascular changes in non-neuropsychiatric systemic lupus erythematosus: A study using diffusion kurtosis imaging and 3D pseudo-continuous arterial spin labeling[J]. J Inflamm Res, 2023, 16: 5465-5475. DOI: 10.2147/JIR.S429521.
[27]
STENBERG J, SKANDSEN T, GØRAN MOEN K, et al. Diffusion tensor and kurtosis imaging findings the first year following mild traumatic brain injury[J]. J Neurotrauma, 2023, 40(5-6): 457-471. DOI: 10.1089/neu.2022.0206.
[28]
WELTON T, HARTONO S, SHIH Y C, et al. Microstructure of brain nuclei in early Parkinson's disease: Longitudinal diffusion kurtosis imaging[J]. J Parkinsons Dis, 2023, 13(2): 233-242. DOI: 10.3233/JPD-225095.
[29]
HU W, QIU Z, HUANG Q, et al. Microstructural changes of the white matter in systemic lupus erythematosus patients without neuropsychiatric symptoms: a multi-shell diffusion imaging study[J/OL].Arthritis Res Ther, 2024, 26(1): 110 [2024-06-14]. https://pubmed.ncbi.nlm.nih.gov/38807248/. DOI: 10.1186/s13075-024-03344-3.
[30]
MA Y Y, DENG M, LI Z F, et al. Three-dimensional arterial spin labeling combined with intravoxel incoherent motionimaging for differential diagnosis of benign and malignant meningiomas[J]. Chin J Med Imaging Technol, 2021, 37(8): 1131-1135. DOI: 10.13929/j.issn.1003-3289.2021.08.003.
[31]
PERCIE DU SERT O, UNRAU J, GAUTHIER C J, et al. Cerebral blood flow in schizophrenia: A systematic review and meta-analysis of MRI-based studies[J/OL]. Prog Neuropsychopharmacol Biol Psychiatry, 2023, 121: 110669 [2024-06-14]. https://doi.org/10.1016/j.pnpbp.2022.110669. DOI: 10.1016/j.pnpbp.2022.110669.
[32]
FERREIRA R, BASTOS-LEITE A J. Arterial spin labelling magnetic resonance imaging and perfusion patterns in neurocognitive and other mental disorders: a systematic review[J]. Neuroradiology, 2024, 66(7): 1065-1081. DOI: 10.1007/s00234-024-03323-0.
[33]
KITAZAKI Y, IKAWA M, YAMAGUCHI T, et al. Regional cortical hypoperfusion and atrophy correlate with striatal dopaminergic loss in Parkinson's disease: a study using arterial spin labeling MR perfusion[J]. Neuroradiology, 2023, 65(3): 569-577. DOI: 10.1007/s00234-022-03085-7.
[34]
JOSHI D, PRASAD S, SAINI J, et al. Role of arterial spin labeling (ASL) images in Parkinson's disease (PD): A systematic review[J]. Acad Radiol, 2023, 30(8): 1695-1708. DOI: 10.1016/j.acra.2022.11.001.
[35]
MENG M, LIU F, MA Y, et al. The identification and cognitive correlation of perfusion patterns measured with arterial spin labeling MRI in Alzheimer's disease[J/OL]. Alzheimers Res Ther, 2023, 15(1): 75 [2024-06-14]. https://doi.org/10.1186/s13195-023-01222-9. DOI: 10.1186/s13195-023-01222-9.
[36]
ZHANG P, LI X L, ZHOU W S, et al. Cerebral blood flow for diagnosis of non-neuropsychiatric systemic lupus erythematosus[J]. Chin J Med Imaging Technol, 2023, 39(1): 22-26. DOI: 10.13929/j.issn.1003-3289.2023.01.005.
[37]
LIU Q, ZHANG X. Multimodality neuroimaging in vascular mild cognitive impairment: A narrative review of current evidence[J/OL]. Front Aging Neurosci, 2023, 15: 1073039 [2024-06-14]. https://doi.org/10.3389/fnagi.2023.1073039. DOI: 10.3389/fnagi.2023.1073039.
[38]
UKADIKE K C, NI K, WANG X, et al. IgG and IgA autoantibodies against L1 ORF1p expressed in granulocytes correlate with granulocyte consumption and disease activity in pediatric systemic lupus erythematosus[J/OL]. Arthritis Res Ther, 2021, 23(1): 153 [2024-06-14]. https://doi.org/10.1186/s13075-021-02538-3. DOI: 10.1186/s13075-021-02538-3.
[39]
ZHUO Z, SU L, DUAN Y, et al. Different patterns of cerebral perfusion in SLE patients with and without neuropsychiatric manifestations[J]. Hum Brain Mapp, 2020, 41(3): 755-766. DOI: 10.1002/hbm.24837.
[40]
PRESA J L, SARAVIA F, BAGI Z, et al. Vasculo-neuronal coupling and neurovascular coupling at the neurovascular unit: Impact of hypertension[J/OL]. Front Physiol, 2020, 11: 584135 [2024-06-14]. https://doi.org/10.3389/fphys.2020.584135. DOI: 10.3389/fphys.2020.584135.
[41]
CLAASSEN J A H R, THIJSSEN D H J, PANERAI R B, et al. Regulation of cerebral blood flow in humans: physiology and clinical implications of autoregulation[J]. Physiol Rev, 2021, 101(4): 1487-1559. DOI: 10.1152/physrev.00022.2020.
[42]
YANG J, GOHEL S, VACHHA B. Current methods and new directions in resting state fMRI[J]. Clin Imaging, 2020, 65: 47-53. DOI: 10.1016/j.clinimag.2020.04.004.
[43]
LIU H H, ZHENG J O. The research progress of methodology of resting state magnetic resonance imaging[J]. Med Recapitulate, 2016, 22(1): 136-140. DOI: 10.3969/j.issn.1006-2084.2016.01.039.
[44]
KARAVALLIL ACHUTHAN S, COBURN K L, BECKERSON M E, et al. Amplitude of low frequency fluctuations during resting state fMRI in autistic children[J]. Autism Res, 2023, 16(1): 84-98. DOI: 10.1002/aur.2846.
[45]
GE X, WANG L, PAN L, et al. Amplitude of low-frequency fluctuation after a single-trigger pain in patients with classical trigeminal neuralgia[J/OL]. J Headache Pain, 2022, 23(1): 117 [2024-06-14]. https://doi.org/10.1186/s10194-022-01488-8. DOI: 10.1186/s10194-022-01488-8.
[46]
YU Y, CHEN L, WANG Q, et al. Altered amplitude of low-frequency fluctuations in inactive patients with nonneuropsychiatric systemic lupus erythematosus[J]. Neural Plast, 2019, 2019: 1-10. DOI: 10.1155/2019/9408612.
[47]
YU H, QIU X, ZHANG Y, et al. Abnormal amplitude of low frequency fluctuation and functional connectivity in non-neuropsychiatric systemic lupus erythematosus: a resting-state fMRI study[J]. Neuroradiology, 2019, 61(3): 331-340. DOI: 10.1007/s00234-018-2138-6.
[48]
PIAO S, WANG R, QIN H, et al. Alterations of spontaneous brain activity in systematic lupus erythematosus patients without neuropsychiatric symptoms: A resting-functional MRI study[J]. Lupus, 2021, 30(11): 1781-1789. DOI: 10.1177/09612033211033984.
[49]
LIN Y H, YOUNG I M, CONNER A K, et al. Anatomy and white matter connections of the inferior temporal gyrus[J/OL]. World Neurosurg, 2020, 143: e656-e666 [2024-06-14]. https://doi.org/10.1016/j.wneu.2020.08.058. DOI: 10.1016/j.wneu.2020.08.058.
[50]
ALAHMADI A A S. Beyond boundaries: investigating shared and divergent connectivity in the pre-/postcentral gyri and supplementary motor area[J]. NeuroReport, 2024, 35(5): 283-290. DOI: 10.1097/WNR.0000000000002011.
[51]
LI X L, ZHOU W S, ZHANG P, et al. Amplitude of low-frequency fluctuations and functional connectivity in non-neuropsychiatric systemic lupus erythematosus: A resting-state functional magneticresonance imaging study[J]. Chin J Med Imaging, 2021, 29(12): 1170-1176. DOI: 10.3969/j.issn.1005-5185.2021.12.002.
[52]
ZHOU Y, ZHU H, HU W, et al. Abnormal regional homogeneity as a potential imaging indicator for identifying adolescent-onset schizophrenia: Insights from resting-state functional magnetic resonance imaging[J/OL]. Asian J Psychiatr, 2024, 98: 104106 [2024-06-14]. https://doi.org/10.1016/j.ajp.2024.104106. DOI: 10.1016/j.ajp.2024.104106.
[53]
LI X, LIU Q, CHEN Z, et al. Abnormalities of regional brain activity in patients with schizophrenia: A longitudinal resting-state fMRI study[J]. Schizophr Bull, 2023, 49(5): 1336-1344. DOI: 10.1093/schbul/sbad054.
[54]
LIU S, CHENG Y, XIE Z, et al. A conscious resting state fMRI study in SLE patients without major neuropsychiatric manifestations[J/OL]. Front Psychiatry, 2018, 9: 677 [2024-06-14]. https://doi.org/10.3389/fpsyt.2018.00677. DOI: 10.3389/fpsyt.2018.00677.
[55]
LI X L, XIA J G, ZOU H M, et al. The changes of brain regional homogeneity in non-NPSLE patients: a resting-statefunctional magnetic resonance imaging study[J].Radiol Pract, 2021, 36(12): 1467-1473. DOI: 10.13609/j.cnki.1000-0313.2021.12.003.
[56]
SALEEM A, HARMATA G, JAIN S, et al. Functional connectivity of the cerebellar vermis in bipolar disorder and associations with mood[J/OL]. bioRxiv [Preprint], 2023: 2023.02.02.526878 [2024-06-14]. https://doi.org/10.1101/2023.02.02.526878. DOI: 10.1101/2023.02.02.526878.
[57]
WANG Y, JIANG M, HUANG L, et al. Altered functional brain network in systemic lupus erythematosus patients without overt neuropsychiatric symptoms based on resting-state functional magnetic resonance imaging and multivariate pattern analysis[J/OL]. Front Neurol, 2021, 12: 690979 [2024-06-14]. https://doi.org/10.3389/fneur.2021.690979. DOI: 10.3389/fneur.2021.690979.
[58]
LI G, ZHANG B, LONG M, et al. Abnormal degree centrality can be a potential imaging biomarker in first-episode, drug-naive bipolar mania[J]. Neuroreport, 2023, 34(6): 323-331. DOI: 10.1097/WNR.0000000000001896.
[59]
ALBERT R, JEONG H, BARABÁSI A L. Error and attack tolerance of complex networks[J]. Nature, 2000, 406(6794): 378-382. DOI: 10.1038/35019019.
[60]
MARKS W D, YAMAMOTO N, KITAMURA T. Complementary roles of differential medial entorhinal cortex inputs to the hippocampus for the formation and integration of temporal and contextual memory (Systems Neuroscience)[J]. Eur J Neurosci, 2021, 54(8): 6762-6779. DOI: 10.1111/ejn.14737.
[61]
NIGRO S, FILARDI M, TAFURI B, et al. The role of graph theory in evaluating brain network alterations in frontotemporal dementia[J/OL]. Front Neurol, 2022, 13: 910054 [2024-06-14]. https://doi.org/10.3389/fneur.2022.910054. DOI: 10.3389/fneur.2022.910054.
[62]
TAN X, LIU X, HAN K, et al. Disrupted resting-state brain functional network properties in non-neuropsychiatric systemic lupus erythematosus patients[J]. Lupus, 2023, 32(4): 538-548. DOI: 10.1177/09612033231160725.

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