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Longitudinal study of multi-parameter quantitative magnetic resonance imaging in Duchenne muscular dystrophy: hyperresponsiveness of gluteus maximus and detection of subclinical disease progression in functionally stable patients

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Abstract

Objective

To describe the disease progression of Duchenne muscular dystrophy (DMD) in the pelvic and thigh muscles over 1-year using multiple-parameter quantitative magnetic resonance imaging (qMRI), and to determine the most responsive muscle and predict subclinical disease progression in functionally stable patients.

Methods

Fifty-four DMD patients (mean age 8.9 ± 2.5, range 5–15 years) completed baseline and 1-year follow-up qMRI examinations/biomarkers [3-point Dixon/fat fraction (FF); T1 mapping/T1; T2 mapping/T2]. Meanwhile, clinical assessments [NorthStar ambulatory assessment (NSAA) score] and timed function tests were performed in DMD patients. Twenty-four healthy male controls (range 5–15 years) accomplished baseline qMRI examinations. Group differences were compared using the Wilcoxon test. The standardized response mean (SRM) was taken as the responsiveness to the disease progression index.

Results

FF, T1, and T2 in all DMD age subgroups changed significantly over 1-year (P < 0.05). Even in functionally stable patients (NSAA score increased, unchanged, or decreased by 1-point) over 1-year, significant increases in FF and T2 and decreases in T1 were observed in gluteus maximus (GMa), gluteus medius, vastus lateralis, and adductor magnus (P < 0.05). Overall, the SRM of FF, T1, and T2 was all the highest in GMa, which were 1.25, − 0.92, and 0.93, respectively.

Conclusions

qMRI biomarkers are responsive to disease progression and can also detect subclinical disease progression in functionally stable DMD patients over 1-year. GMa is the most responsive to disease progression of all the muscles analyzed.

Trial registration

Chinese Clinical Trial Registry (http://www.chictr.org.cn/index.aspx) ChiCTR1800018340, 09/12/2018, prospectively registered.

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Funding

This work was supported by National Natural Science Foundation of China (Grand Nos. 81860316, 81971586, 82071874, 81901712, 821201080105); Jiangxi Provincial key Natural Science Foundation of China (20212ACB206021); Sichuan Science and Technology Program (21ZDYF1967); Clinical Research Finding of Chinese Society of Cardiovascular Disease (CSC) of 2019 (No. HFCSC2019B01); and Fellowship of China postdoctoral science foundation (2021M692290).

Author information

Author notes

  1. Fei Peng and Huayan Xu have contributed equally to this work.

  2. Xiaotang Cai, Yingkun Guo and Lianggeng Gong have contributed equally to the correspondence.

Authors and Affiliations

  1. Department of Medical Imaging Center, The Second Affiliated Hospital of Nanchang University, Minde Road No. 1, Nanchang, 330006, Jiangxi Province, China

    Fei Peng, Shuhao Li & Lianggeng Gong

  2. Department of Radiology, Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, 20# Section 3 South Renmin Road, Chengdu, 610041, Sichuan Province, China

    Fei Peng, Huayan Xu, Yu Song, Ke Xu & Yingkun Guo

  3. Department of Pediatrics Neurology, West China Second University Hospital, Sichuan University, 20# Section 3 South Renmin Road, Chengdu, 610041, Sichuan Province, China

    Xiaotang Cai

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  1. Fei Peng
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Contributions

FP and HX participated in the study design, contributed to data analysis and interpretation, statistical analysis, and drafted the main manuscript, and are the co-first authors.‍ YS and KX carried out data acquisition and contributed to image quality controlling.‍ SL contributed to editing and review of the manuscript. XC, YG, and LG participated in the whole study design, contributed to quality control of data and algorithms, editing and review of the manuscript, and are the co-corresponding authors.‍ All authors contributed to the article and approved the submitted version.

Corresponding authors

Correspondence to Xiaotang Cai, Yingkun Guo or Lianggeng Gong.

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Ethical standard statement

This study was approved by the local Institutional Review Board and performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

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Written informed consent was acquired from all participants and guardians before study participation.

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Peng, F., Xu, H., Song, Y. et al. Longitudinal study of multi-parameter quantitative magnetic resonance imaging in Duchenne muscular dystrophy: hyperresponsiveness of gluteus maximus and detection of subclinical disease progression in functionally stable patients. J Neurol 270, 1439–1451 (2023). https://doi.org/10.1007/s00415-022-11470-8

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  • DOI: https://doi.org/10.1007/s00415-022-11470-8

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