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U-fiber diffusion kurtosis and susceptibility characteristics in relapsing–remitting multiple sclerosis may be related to cognitive deficits and neurodegeneration

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Abstract

Objectives

To evaluate the diffusion kurtosis and susceptibility change in the U-fiber region of patients with relapsing–remitting multiple sclerosis (pwRRMS) and their correlations with cognitive status and degeneration.

Materials and methods

Mean kurtosis (MK), axial kurtosis (AK), radial kurtosis (RK), kurtosis fractional anisotropy (KFA), and the mean relative quantitative susceptibility mapping (mrQSM) values in the U-fiber region were compared between 49 pwRRMS and 48 healthy controls (HCs). The U-fiber were divided into upper and deeper groups based on the location. The whole brain volume, gray and white matter volume, and cortical thickness were obtained. The correlations between the mrQSM values, DKI-derived metrics in the U-fiber region and clinical scale scores, brain morphologic parameters were further investigated.

Results

The decreased MK, AK, RK, KFA, and increased mrQSM values in U-fiber lesions (p < 0.001, FDR corrected), decreased RK, KFA, and increased mrQSM values in U-fiber non-lesions (p = 0.034, p < 0.001, p < 0.001, FDR corrected) were found in pwRRMS. There were differences in DKI-derived metrics and susceptibility values between the upper U-fiber region and the deeper one for U-fiber non-lesion areas of pwRRMS and HCs (p < 0.05), but not for U-fiber lesions in DKI-derived metrics. The DKI-derived metrics and susceptibility values were widely related with cognitive tests and brain atrophy.

Conclusion

RRMS patients show abnormal diffusion kurtosis and susceptibility characteristics in the U-fiber region, and these underlying tissue abnormalities are correlated with cognitive deficits and degeneration.

Clinical relevance statement

The macroscopic and microscopic tissue damages of U-fiber help to identify cognitive impairment and brain atrophy in multiple sclerosis and provide underlying pathophysiological mechanism.

Key Points

• Diffusion kurtosis and susceptibility changes are present in the U-fiber region of multiple sclerosis.

• There are gradients in diffusion kurtosis and susceptibility characteristics in the U-fiber region.

• Tissue damages in the U-fiber region are correlated with cognitive impairment and brain atrophy.

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Abbreviations

AK:

Axial kurtosis

DKI:

Diffusion kurtosis imaging

DST:

Digit Span Test

DTI:

Diffusion tensor imaging

DWM:

Deep white matter

EDSS:

Expanded Disability Status Scale

FLAIR:

Fluid-attenuated inversion recovery

FSS:

Fatigue Severity Scale

HAMD:

Hamilton Depression

HCs:

Healthy controls

KFA:

Kurtosis fractional anisotropy

MK:

Mean kurtosis

MoCA:

Montreal Cognitive Assessment

MPRAGE:

Magnetization prepared rapid gradient echo

MRI:

Magnetic resonance imaging

mrQSM:

Mean relative quantitative susceptibility mapping

MS:

Multiple sclerosis

NAWM:

Normal-appearing white matter

Non-UFLs:

U-fiber non-lesions

pwRRMS:

Patients with relapsing–remitting multiple sclerosis

QSM:

Quantitative susceptibility mapping

RK:

Radial kurtosis

RRMS:

Relapsing-remitting MS

SDMT:

Symbol Digit Modalities Test

SWM:

Superficial white matter

UFLs:

U-fiber lesions

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Funding

This study received grants from the Key Project of Technological Innovation and Application Development of Chongqing Science and Technology Bureau (CSTC2021 jscx-gksb-N0008).

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Authors and Affiliations

  1. Department of Radiology, the First Affiliated Hospital of Chongqing Medical University, No. 1 Youyi Road, Yuzhong District, Chongqing, 400016, China

    Dan Luo, Yuling Peng, Qiyuan Zhu, Qiao Zheng, Qi Luo, Yongliang Han, Xiaoya Chen & Yongmei Li

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  1. Dan Luo
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  2. Yuling Peng
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  3. Qiyuan Zhu
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  4. Qiao Zheng
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Correspondence to Xiaoya Chen or Yongmei Li.

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The scientific guarantor of this publication is Yongmei Li.

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The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

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Written informed consent was obtained from all participants.

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This retrospective study was approved by the Institutional Review Board of the First Affiliated Hospital of Chongqing Medical University.

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• Retrospective

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• Performed at one institution

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Luo, D., Peng, Y., Zhu, Q. et al. U-fiber diffusion kurtosis and susceptibility characteristics in relapsing–remitting multiple sclerosis may be related to cognitive deficits and neurodegeneration. Eur Radiol 34, 1422–1433 (2024). https://doi.org/10.1007/s00330-023-10114-3

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