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. 2024 May 28;26(1):110.
doi: 10.1186/s13075-024-03344-3.

Microstructural changes of the white matter in systemic lupus erythematosus patients without neuropsychiatric symptoms: a multi-shell diffusion imaging study

Wenjun Hu #  1 , Ziru Qiu #  2   3 , Qin Huang  4 , Yuhao Lin  5 , Jiaying Mo  1 , Linhui Wang  1 , Jingyi Wang  1 , Kan Deng  6 , Yanqiu Feng  2   3 , Xinyuan Zhang  7   8 , Xiangliang Tan  9
Affiliations

Microstructural changes of the white matter in systemic lupus erythematosus patients without neuropsychiatric symptoms: a multi-shell diffusion imaging study

Wenjun Hu et al. Arthritis Res Ther. .

Abstract

Background: Diffusion kurtosis imaging (DKI) and neurite orientation dispersion and density imaging (NODDI) provide more comprehensive and informative perspective on microstructural alterations of cerebral white matter (WM) than single-shell diffusion tensor imaging (DTI), especially in the detection of crossing fiber. However, studies on systemic lupus erythematosus patients without neuropsychiatric symptoms (non-NPSLE patients) using multi-shell diffusion imaging remain scarce.

Methods: Totally 49 non-NPSLE patients and 41 age-, sex-, and education-matched healthy controls underwent multi-shell diffusion magnetic resonance imaging. Totally 10 diffusion metrics based on DKI (fractional anisotropy, mean diffusivity, axial diffusivity, radial diffusivity, mean kurtosis, axial kurtosis and radial kurtosis) and NODDI (neurite density index, orientation dispersion index and volume fraction of the isotropic diffusion compartment) were evaluated. Tract-based spatial statistics (TBSS) and atlas-based region-of-interest (ROI) analyses were performed to determine group differences in brain WM microstructure. The associations of multi-shell diffusion metrics with clinical indicators were determined for further investigation.

Results: TBSS analysis revealed reduced FA, AD and RK and increased ODI in the WM of non-NPSLE patients (P < 0.05, family-wise error corrected), and ODI showed the best discriminative ability. Atlas-based ROI analysis found increased ODI values in anterior thalamic radiation (ATR), inferior frontal-occipital fasciculus (IFOF), forceps major (F_major), forceps minor (F_minor) and uncinate fasciculus (UF) in non-NPSLE patients, and the right ATR showed the best discriminative ability. ODI in the F_major was positively correlated to C3.

Conclusion: This study suggested that DKI and NODDI metrics can complementarily detect WM abnormalities in non-NPSLE patients and revealed ODI as a more sensitive and specific biomarker than DKI, guiding further understanding of the pathophysiological mechanism of normal-appearing WM injury in SLE.

Keywords: Atlas-based region-of-interest (ROI) analysis; Diffusion kurtosis imaging; Neurite orientation dispersion and density imaging; Systemic lupus erythematosus; Tract-based spatial statistics.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
TBSS and ROC curve analyses. (A) TBSS analysis showed clusters of significant differences in DKI (FA, AD and RK) and NODDI (ODI) metrics between non-NPSLE patients and the healthy group (P < 0.05, FWE corrected). FA: Fractional Anisotropy; AD: Axial Diffusivity; RK: Radial Kurtosis; ODI: Orientation Dispersion Index. Red and blue denote increase and decrease in the non-NPSLE group, respectively. The superscript number in each image refers to its slice. (B) Receiver operating characteristic (ROC) curves of averaged FA, AD, RK and ODI values in each significant cluster identified by tract-based spatial statistics analysis (TBSS). AUC, Area under the ROC Curve
Fig. 2
Fig. 2
Atlas-based ROI and ROC curve analyses. (A) Atlas-based region of interested (ROI) analysis of the non-NPSLE group versus healthy controls. Mean ODI values of left/right significant JHU tracts in the Student’s t test with FDR correction. Scatterplots show the mean ODI values of various JHU tracts for each participant. Boxplots show median, mean, minimum, maximum and interquartile range. *P < 0.05 (two-tailed), **P < 0.01 (two-tailed). L: Left; R: Right; ATR: Anterior Thalamic Radiation; F_minor: Forceps Minor; F_major: Forceps Major; IFOF: Inferior Fronto-occipital Fasciculus; UF: Uncinate Fasciculus. (B) Receiver operating characteristic (ROC) curves for averaged orientation dispersion index (ODI) values in significant John Hopkins University (JHU) tracts. AUC: Area under the ROC Curve
Fig. 3
Fig. 3
C3 shows a positive correlation with ODI in F_major. Spearman correlation analysis of C3 and F_major of orientation dispersion index (ODI) in the non-NPSLE group. Average ODI in F_major correlated positively with C3 value. F_major: Forceps Major
See this image and copyright information in PMC

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