Share：
Share this content in WeChat
X
[Chinese] [PDF] 582 1
• Clinical Article •
Application of 3D-ASL in assessing cerebral blood flow perfusion in patients with neuropsychiatric systemic lupus erythematosus
AN Ning  MA Yue  ZHAO Ruiting  MA Xueying  QIAO Pengfei 

Cite this article as: AN N, MA Y, ZHAO R T, et al. Application of 3D-ASL in assessing cerebral blood flow perfusion in patients with neuropsychiatric systemic lupus erythematosus[J]. Chin J Magn Reson Imaging, 2025, 16(9): 15-21. DOI:10.12015/issn.1674-8034.2025.09.003.


[Abstract] Objective To investigate the correlation between changes in cerebral perfusion patterns and serum immunological markers as well as cognitive assessments in patients with neuropsychiatric systemic lupus erythematosus (NPSLE) using three-dimensional arterial spin labeling (3D-ASL) technology, and to explore the pathogenesis of NPSLE from an imaging perspective.Materials and Methods Prospectively collected imaging, clinical serological, and cognitive assessment data from 37 NPSLE patients, 52 non-neuropsychiatric systemic lupus erythematosus (non-NPSLE) patients, and 39 healthy controls (HC) were analyzed. Differences in cerebral perfusion patterns were compared, and correlation analyses were conducted between cerebral blood flow (CBF) values in differentially perfused brain regions of NPSLE patients and serum/cognitive indicators.Results CBF differences revealed that the NPSLE group exhibited significantly higher CBF in the left middle temporal gyrus and left supramarginal gyrus compared to the non-NPSLE group (P < 0.001). Compared to the HC group, the NPSLE group showed increased CBF in the aforementioned regions as well as decreased CBF in multiple brain areas, including the right superior frontal gyrus (P < 0.001). Correlation analysis demonstrated that in NPSLE patients, CBF values in the left middle temporal gyrus were positively correlated with hemoglobin (r = 0.392, P = 0.037), red blood cell count (r = 0.437, P = 0.022), and visuospatial/executive function scores on the Montreal Cognitive Assessment (MoCA) (r = 0.358, P = 0.016), while negatively correlated with anxiety scale scores (r = -0.380, P = 0.015). CBF values in the left supramarginal gyrus were positively correlated with hemoglobin (r = 0.612, P = 0.016), hematocrit (r = 0.457, P = 0.016), and complement 3 (r = 0.538, P = 0.008), but negatively correlated with beck anxiety inventory (BAI) scores (r = -0.397, P = 0.040).Conclusions Patients with NPSLE have abnormal cerebral perfusion patterns. These changes may play a key role in the pathophysiological process of neuropsychiatric symptoms in patients with NPSLE and are involved in the occurrence and development of its pathological mechanism.
[Keywords] neuropsychiatric systemic lupus erythematosus；cerebral blood flow；cognitive dysfunction；three-dimensional arterial spin labeling；magnetic resonance imaging

AN Ning1, 2   MA Yue3   ZHAO Ruiting4   MA Xueying2   QIAO Pengfei2*  

1 The First Clinical Medical College of Inner Mongolia Medical University, Hohhot 010000, China

2 Department of Imaging Diagnosis, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot 010000, China

3 Department of Medical Imaging, Inner Mongolia Aerospace Hospital, Hohhot 010000, China

4 Imaging Center of Inner Mongolia Autonomous Region Third Hospital, Hohhot 010000, China

Corresponding author: QIAO P F, E-mail: 24853170@qq.com

Conflicts of interest   None.

Received  2025-03-19
Accepted  2025-08-05
DOI: 10.12015/issn.1674-8034.2025.09.003
Cite this article as: AN N, MA Y, ZHAO R T, et al. Application of 3D-ASL in assessing cerebral blood flow perfusion in patients with neuropsychiatric systemic lupus erythematosus[J]. Chin J Magn Reson Imaging, 2025, 16(9): 15-21. DOI:10.12015/issn.1674-8034.2025.09.003.

[1]
DE AMORIM J C, FRITTOLI R B, PEREIRA D, et al. Epidemiology, characterization, and diagnosis of neuropsychiatric events in systemic lupus erythematosus[J]. Expert Rev Clin Immunol, 2019, 15(4): 407-416. DOI: 10.1080/1744666X.2019.1564040.
[2]
OTA Y, SRINIVASAN A, CAPIZZANO A A, et al. Central Nervous System Systemic Lupus Erythematosus: Pathophysiologic, Clinical, and Imaging Features[J]. Radiographics, 2022, 42(1): 212-232. DOI: 10.1148/rg.210045.
[3]
LEGGE A C, HANLY J G. Recent advances in the diagnosis and management of neuropsychiatric lupus[J]. Nat Rev Rheumatol, 2024, 20(11): 712-728. DOI: 10.1038/s41584-024-01163-z.
[4]
CHOJDAK-ŁUKASIEWICZ J, DZIADKOWIAK E, ZIMNY A, et al. Cerebral small vessel disease: A review[J]. Adv Clin Exp Med, 2021, 30(3): 349-356. DOI: 10.17219/acem/131216.
[5]
SOLLMANN N, HOFFMANN G, SCHRAMM S, et al. Arterial Spin Labeling (ASL) in Neuroradiological Diagnostics - Methodological Overview and Use Cases[J]. Rofo, 2024, 196(1): 36-51. DOI: 10.1055/a-2119-5574.
[6]
LI X Y, TIAN Y T, WANG X N, et al. Cerebral perfusion in Parkinson's disease with depression: An arterial spin labeling MRI study[J]. Chin J Magn Reson Imaging, 2023, 14(1): 6-12. DOI: 10.12015/issn.1674-8034.2023.01.002.
[7]
WANG X W, WU F, LIU Y H, et al. Study of pseudo-continuous arterial spin labeling perfusion MRI on the evaluation of cerebral hemodynamics in patients with hemorrhagic moyamoya disease[J]. Chin J Magn Reson Imaging, 2022, 13(1): 6-10. DOI: 10.12015/issn.1674-8034.2022.01.002.
[8]
WANG X, BISHOP C, O'CALLAGHAN J, et al. MRI assessment of cerebral perfusion in clinical trials[J/OL]. Drug Discov Today, 2023, 28(4): 103506 [2025-03-19]. https://doi.org/10.1016/j.drudis.2023.103506. DOI: 10.1016/j.drudis.2023.103506.
[9]
SIEGEL C H, SAMMARITANO L R. Systemic Lupus Erythematosus: A Review[J]. JAMA, 2024, 331(17): 1480-1491.
[10]
American College of Rheumatology. 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.
[11]
NASREDDINE Z S, PHILLIPS N A, BÉDIRIAN V, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment[J]. J Am Geriatr Soc, 2005, 53(4): 695-699. DOI: 10.1111/j.1532-5415.2005.53221.x.
[12]
NIKOLOPOULOS D, MANOLAKOU T, POLISSIDIS A, et al. Microglia activation in the presence of intact blood-brain barrier and disruption of hippocampal neurogenesis via IL-6 and IL-18 mediate early diffuse neuropsychiatric lupus[J]. Ann Rheum Dis, 2023, 82(5): 646-657. DOI: 10.1136/ard-2022-223506.
[13]
MOORE E, HUANG M W, REYNOLDS C A, et al. Choroid Plexus-Infiltrating T Cells as Drivers of Murine Neuropsychiatric Lupus[J]. Arthritis Rheumatol, 2022, 74(11): 1796-1807. DOI: 10.1002/art.42252.
[14]
YAN H M, WU Y Q, DENG X J, et al. Research progress of immunological pathogenesis and commonly used animal models of neuropsychiatric systemic lupus erythematosus[J]. Chinese Journal of Pathophysiology, 2022, 38(2): 333-341. DOI: 10.3969/j.issn.1000-4718.2022.02.018.
[15]
ZABALA A, SALGUEIRO M, SÁEZ-ATXUKARRO O, et al. Cognitive Impairment in Patients With Neuropsychiatric and Non-neuropsychiatric Systemic Lupus Erythematosus: A Systematic Review and Meta-analysis[J]. J Int Neuropsychol Soc, 2018, 24(6): 629-639. DOI: 10.1017/S1355617718000073.
[16]
ZHU C M, MA Y, XIE L, et al. Spatial Working Memory Impairment in Patients with Non-neuropsychiatric Systemic Lupus Erythematosus: A Blood-oxygen-level Dependent Functional Magnetic Resonance Imaging Study[J]. J Rheumatol, 2017, 44(2): 201-208. DOI: 10.3899/jrheum.160290.
[17]
SUNTOKO B, HADISAPUTRO S, KALIM H, et al. Relationship Between Disease Activity, Levels of IFN-a, IL-4, IL-6, and Anti-NMDA to Cognitive Dysfunction (MoCA-INA Score) in Systemic Lupus Erythematosus (SLE) Patients with Cognitive Dysfunction[J]. Acta Med Indones, 2023, 55(3): 307-314.
[18]
CARROLL K R, MIZRACHI M, SIMMONS S, et al. Lupus autoantibodies initiate neuroinflammation sustained by continuous HMGB1:RAGE signaling and reversed by increased LAIR-1 expression[J]. Nat Immunol, 2024, 25(4): 671-681. DOI: 10.1038/s41590-024-01772-6.
[19]
LI M G, CHEN Y Y, CHEN Z Y, et al. Altered functional connectivity of the marginal division in Parkinson's disease with mild cognitive impairment: A pilot resting-state fMRI study[J]. J Magn Reson Imaging, 2019, 50(1): 183-192. DOI: 10.1002/jmri.26548.
[20]
LUO Y, QIAO M, LIANG Y, et al. Functional Brain Connectivity in Mild Cognitive Impairment With Sleep Disorders: A Study Based on Resting-State Functional Magnetic Resonance Imaging[J/OL]. Front Aging Neurosci, 2022, 14: 812664 [2025-03-19]. https://doi.org/10.3389/fnagi.2022.812664. DOI: 10.3389/fnagi.2022.812664.
[21]
TANG Y F, ZANG C, MIAO Y Y. Clinical Value of Magnetic Resonance Arterial Spin Labeling in the Diagnosis of Nonvascular and Vascular Mild Cognitive Impairment[J]. Henan Medical Research, 2023, 32(16): 3039-3042. DOI: 10.3969/j.issn.1004-437X.2023.16.039.
[22]
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 [2025-03-19]. https://doi.org/10.1186/s13195-023-01222-9. DOI: 10.1186/s13195-023-01222-9.
[23]
LIU H, LIU H, TIAN B, et al. Alterations in cerebral perfusion and corresponding brain functional networks in systemic lupus erythematosus with cognitive impairment[J/OL]. Sci Rep, 2025, 15(1): 1310 [2025-03-19]. https://doi.org/10.1038/s41598-025-85648-1. DOI: 10.1038/s41598-025-85648-1.
[24]
HUANG C J, YUAN X, ZHANG W, et al. Altered neurovascular coupling in arteriosclerotic cerebral small vessel disease and the correlation with cognitive function[J]. Chin J Neurol, 2022, 55(5): 458-465. DOI: 10.3760/cma.j.cn113694-20211110-00792.
[25]
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.
[26]
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 [2025-03-19]. https://doi.org/10.3389/fneur.2021.690979. DOI: 10.3389/fneur.2021.690979.
[27]
GUEYE M, PREZIOSA P, RAMIREZ G A, et al. Choroid plexus and perivascular space enlargement in neuropsychiatric systemic lupus erythematosus[J]. Mol Psychiatry, 2024, 29(2): 359-368. DOI: 10.1038/s41380-023-02332-4.
[28]
JIA J, XIE J, LI H, et al. Cerebral blood flow abnormalities in neuropsychiatric systemic lupus erythematosus[J]. Lupus, 2019, 28(9): 1128-1133. DOI: 10.1177/0961203319861677.
[29]
HENRIKSEN O M, GJEDDE A, VANG K, et al. Regional and interindividual relationships between cerebral perfusion and oxygen metabolism[J]. J Appl Physiol (1985), 2021, 130(6): 1836-1847. DOI: 10.1152/japplphysiol.00939.2020.
[30]
LIU J, JIA S Y, WANG P Y, et al. Analysis of clinical characteristics and risk factors in patients with neuropsychiatric systemic lupus erythematosus(NPSLE)[J]. Chin J Cell Mol Immunol, 2023, 39(10): 924-927. DOI: 1007-8738(2023)10-0924-04.
[31]
DUARTE-DELGADO N P, VÁSQUEZ G, ORTIZ-REYES B L. Blood-brain barrier disruption and neuroinflammation as pathophysiological mechanisms of the diffuse manifestations of neuropsychiatric systemic lupus erythematosus[J]. Autoimmun Rev, 2019, 18(4): 426-432. DOI: 10.1016/j.autrev.2018.12.004.
[32]
PEKNA M, PEKNY M. The Complement System: A Powerful Modulator and Effector of Astrocyte Function in the Healthy and Diseased Central Nervous System[J/OL]. Cells, 2021, 10(7): 1812 [2025-03-19]. https://doi.org/10.3390/cells10071812. DOI: 10.3390/cells10071812.
[33]
PAPADAKI E, KAVROULAKIS E, BERTSIAS G, et al. Regional cerebral perfusion correlates with anxiety in neuropsychiatric SLE: evidence for a mechanism distinct from depression[J]. Lupus, 2019, 28(14): 1678-1689. DOI: 10.1177/0961203319887793.
[34]
MESULAM M M. Temporopolar regions of the human brain[J]. Brain, 2023, 146(1): 20-41. DOI: 10.1093/brain/awac339.
[35]
LIU J, SPAGNA A, BARTOLOMEO P. Hemispheric asymmetries in visual mental imagery[J]. Brain Struct Funct, 2022, 227(2): 697-708. DOI: 10.1007/s00429-021-02277-w.
[36]
GAO D Y, WANG Y, WANG X, et al. Exploring the Correlation between White Matter Hyperintensity, White Matter Hyperintensity Penumbra and Cognitive Impairment in Cerebral Sm all Vessel Disease Based on 3D-ASL and DKI Sequences[J]. Chin J Stroke, 2024, 19(8): 931-937. DOI: 10.3969/j.issn.1673-5765.2024.08.011.

PREV Modulation of triple network connectivity in premenstrual syndrome by transcutaneous auricular vagus nerve stimulation: A fMRI study
NEXT Analysis of MR imaging evolution and related factors of recent small subcortical infarcts with cerebral small vessel disease
  


LINK


Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn