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Immune-related visual dysfunction in thyroid eye disease: a combined orbital and brain neuroimaging study

  • Magnetic Resonance
  • Published:
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Abstract

Objectives

To investigate the pathological interplay between immunity and the visual processing system (VPS) in thyroid eye disease (TED).

Methods

A total of 24 active patients (AP), 26 inactive patients (IP) of TED, and 27 healthy controls (HCs) were enrolled. Orbital magnetic resonance imaging (MRI) and resting-state functional MRI (rs-fMRI) were conducted for each participant. Multiple MRI parameters of the intraorbital optic nerve (ON) were assessed. The amplitude of low-frequency fluctuations (ALFF) and regional homogeneity (ReHo) were calculated. Correlation analyses were carried out on the above parameters and clinical characteristics.

Results

Visual functioning scores differentiated between the AP and IP groups. The ON subarachnoid space and ON sheath diameter were significantly higher in AP than in IP. Six vision-related brain regions were identified in TED patients compared with HCs, including right calcarine (CAL.R), right cuneus (CUN.R), left postcentral gyrus (PoCG.L), right middle temporal gyrus (MTG.R), left superior frontal gyrus (SFG.L), and left caudate (CAU.L). The brain activity of MTG.R, SFG.L, and CAU.L differentiated between the AP and IP groups. The correlation analysis revealed a close association among the vision-related brain regions, MRI parameters of ON, and clinical characteristics in AP and IP, respectively.

Conclusions

Combined orbital and brain neuroimaging revealed abnormalities of the VPS in TED, which had a close correlation with immune statuses. Vision-related brain regions in TED might be possibly altered by peripheral immunity via a direct or indirect approach.

Clinical relevance statement

The discovery of this study explained the disparity of visual dysfunction in TED patients with different immune statuses. With the uncovered neuroimaging markers, early detection and intervention of visual dysfunction could be achieved and potentially benefit TED patients.

Key Points

• Patients with different immune statuses of thyroid eye disease varied in the presentation of visual dysfunction.

• The combined orbital and brain neuroimaging study identified six altered vision-related brain regions, which had a significant correlation with the MRI parameters of the intraorbital optic nerve and immunological characteristics.

• Peripheral immunity might possibly give rise to alterations in the central nervous system part of the visual processing system via a direct or indirect approach.

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Abbreviations

ALFF:

Amplitude of low-frequency fluctuation

CAL.R:

Right calcarine fissure

CAU.L:

Left caudate nucleus

CUN.R:

Right cuneus

DON:

Dysthyroid optic neuropathy

FF:

Fat fraction

MRI:

Magnetic resonance imaging

MTG.R:

Right temporal middle gyrus

ON:

Optic nerve

ONSD:

Optic nerve sheath diameter

PoCG.L:

Left postcentral gyrus

ReHo:

Regional homogeneity

rs-fMRI:

Resting-state functional magnetic resonance imaging

SFG.L:

Left frontal superior gyrus

TED:

Thyroid eye disease

VPS:

Visual processing system

WF:

Water fraction

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Acknowledgements

We would like to thank technique professionals from Shanghai Medoo Tech Company. We also extend our gratitude to Qingwen Tang, Qi Zheng, and Hui Liu for their excellent data collation work.

Funding

This work was supported by the National Natural Science Foundation of China (81930024, 82071003, 82000879, 82271072, and 82271122); the Science and Technology Commission of Shanghai (20DZ22708); Shanghai Key Clinical Specialty, Shanghai Eye Disease Research Center (2022ZZ01003); Clinical Research Plan of SHDC (SHDC2020CR3051B); Clinical Acceleration Program of Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine (JYLJ202202); Cross disciplinary Research Fund of Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine (JYJC202115).

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  1. Haiyang Zhang and Yuting Liu are the co-first authors that have equal contributions

Authors and Affiliations

  1. Department of Ophthalmology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Haiyang Zhang, Yuting Liu, Feiyang Shen, Tianyi Zhu, Jipeng Li, Sijie Fang, Yinwei Li, Jing Sun, Xuefei Song, Huifang Zhou & Xianqun Fan

  2. Shanghai Key Laboratory of Orbital Diseases and Ocular Oncology, Shanghai, China

    Haiyang Zhang, Yuting Liu, Feiyang Shen, Tianyi Zhu, Jipeng Li, Sijie Fang, Yinwei Li, Jing Sun, Xuefei Song, Huifang Zhou & Xianqun Fan

  3. Department of Radiology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Mengda Jiang

  4. School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai, China

    Duojin Xia

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  1. Haiyang Zhang
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Correspondence to Xuefei Song, Huifang Zhou or Xianqun Fan.

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The scientific guarantor of this publication is Xianqun Fan.

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Zhang, H., Liu, Y., Jiang, M. et al. Immune-related visual dysfunction in thyroid eye disease: a combined orbital and brain neuroimaging study. Eur Radiol (2023). https://doi.org/10.1007/s00330-023-10309-8

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