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Spinal cord and brain atrophy patterns in neuromyelitis optica spectrum disorder and multiple sclerosis

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Abstract

Background

Spinal cord and brain atrophy are common in neuromyelitis optica spectrum disorder (NMOSD) and relapsing-remitting multiple sclerosis (RRMS) but harbor distinct patterns accounting for disability and cognitive impairment.

Methods

This study included 209 NMOSD and 304 RRMS patients and 436 healthy controls. Non-negative matrix factorization was used to parse differences in spinal cord and brain atrophy at subject level into distinct patterns based on structural MRI. The weights of patterns were obtained using a linear regression model and associated with Expanded Disability Status Scale (EDSS) and cognitive scores. Additionally, patients were divided into cognitive impairment (CI) and cognitive preservation (CP) groups.

Results

Three patterns were observed in NMOSD: (1) Spinal Cord-Deep Grey Matter (SC-DGM) pattern was associated with high EDSS scores and decline of visuospatial memory function; (2) Frontal-Temporal pattern was associated with decline of language learning function; and (3) Cerebellum-Brainstem pattern had no observed association. Patients with CI had higher weights of SC-DGM pattern than CP group. Three patterns were observed in RRMS: (1) DGM pattern was associated with high EDSS scores, decreased information processing speed, and decreased language learning and visuospatial memory functions; (2) Frontal-Temporal pattern was associated with overall cognitive decline; and (3) Occipital pattern had no observed association. Patients with CI trended to have higher weights of DGM and Frontal-Temporal patterns than CP group.

Conclusion

This study estimated the heterogeneity of spinal cord and brain atrophy patterns in NMOSD and RRMS patients at individual level, and evaluated the clinical relevance of these patterns, which may contribute to stratifying participants for targeted therapy.

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Data availability

The data can be made available upon reasonable request by a qualified researcher.

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Acknowledgements

We acknowledge the contribution of colleagues and patients who participated in this multicenter study.

Funding

National Science Foundation of China, Grant/Award Numbers: 82202084; Beijing Hospital Management Center Young Talents, Grant/Award Numbers: QML20210505; Young Scientists Program of Beijing Tiantan Hospital, Capital Medical University; National Science Foundation of China, Grant/Award Numbers: 82330057.

Author information

Author notes

  1. Tiantian Hua, and Houyou Fan were first authors, who contributed equally to this work.

  2. Zhizheng Zhuo, Xinghu Zhang and Yaou Liu were senior authors, who contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, Beijing Tiantan Hospital, No. 119 South 4th Ring West Road, Fengtai District, Beijing, 100070, China

    Tiantian Hua, Yunyun Duan, Xiaolu Xu, Yuna Li, Siyao Xu, Ying Jin, Hongfang Li, Zhizheng Zhuo & Yaou Liu

  2. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Houyou Fan & Yutong Bai

  3. Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, 100070, People’s Republic of China

    Decai Tian & Xinghu Zhang

  4. Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, School of Biomedical Engineering, Capital Medical University, Beijing, China

    Zhenpeng Chen

  5. Department of Radiology and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, China

    Ningnannan Zhang & Jie Sun

  6. Department of Radiology, Huashan Hospital Fudan University, Shanghai, China

    Haiqing Li & Yuxin Li

  7. Department of Radiology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China

    Yongmei Li & Chun Zeng

  8. Department of Neurology, China−Japan Union Hospital of Jilin University, Changchun, China

    Xuemei Han

  9. Department of Radiology, The First Affiliated Hospital of Nanchang University, Nanchang, China

    Fuqing Zhou & Muhua Huang

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  1. Tiantian Hua
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Contributions

Yaou Liu was the guarantor of integrity of the entire study and contributed to study concepts; Tiantian Hua and Houyou Fan contributed to study design, statistical analyses, and manuscript preparation; Yaou Liu, Tiantian Hua, Zhizheng Zhuo, Houyou Fan, Zhenpeng Chen, and Yutong Bai contributed to definition of intellectual content; Yunyun Duan created the lesion mask. Tiantian Hua, Zhizheng Zhuo, and Yaou Liu contributed to literature research; Xiaolu Xu, Yuna Li, Ningnannan Zhang, Jie Sun, Haiqing Li, Yuxin Li, Yongmei Li, Chun Zeng, Xuemei Han, Fuqing Zhou, Muhua Huang, Siyao Xu, Ying Jin, and Hongfang Li, contributed to data acquisition; Zhizheng Zhuo and Houyou Fan contributed to data analysis; Tiantian Hua, and Zhizheng Zhuo contributed to manuscript editing; Yaou Liu and Xinghu Zhang contributed to manuscript review.

Corresponding author

Correspondence to Yaou Liu.

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Conflicts of interest

The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: Tiantian Hua, Houyou Fan, Yunyun Duan, Decai Tian, Zhenpeng Chen, Xiaolu Xu, Yutong Bai, Yuna Li, Ningnannan Zhang, Jie Sun, Haiqing Li, Yuxin Li, Yongmei Li, Chun Zeng, Xuemei Han, Fuqing Zhou, Muhua Huang, Siyao Xu, Ying Jin, Hongfang Li, Zhizheng Zhuo, Xinghu Zhang, and Yaou Liu declare that there is no conflict of interest.

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Hua, T., Fan, H., Duan, Y. et al. Spinal cord and brain atrophy patterns in neuromyelitis optica spectrum disorder and multiple sclerosis. J Neurol (2024). https://doi.org/10.1007/s00415-024-12281-9

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