Share this content in WeChat
Research progress of magnetic resonance imaging in the assessment of TAO activity
ZHANG Yingcong  BI Qiu  GONG Xiarong  ZHANG Jie  LI Qingrui  WANG Qian  LI Chenrong  CHENG Changxin 

ZHANG Y C, BI Q, GONG X R, et al. Research progress of magnetic resonance imaging in the assessment of TAO activity[J]. Chin J Magn Reson Imaging, 2023, 14(9): 125-130. DOI:10.12015/issn.1674-8034.2023.09.023.

[Abstract] Thyroid-associated ophthalmopathy (TAO) is an autoimmune orbital disease. TAO affects the patient's appearance and even causes blindness, which reduces the patient's quality of life. The assessment of its disease activity and symptom severity is the basis for formulating treatment plans. Clinical activity score is mainly used to evaluate the stage of TAO. The imaging manifestations of TAO patients are mainly exophthalmos, extraocular myoedema thickening and orbital lipopedema, and other manifestations may be combined with enlarged tear gland volume, eyelid and optic nerve edema. Multi-modal MRI techniques such as T2WI fat suppression sequence, dynamic enhanced MRI, diffusion magnetic resonance imaging, mapping, magnetization transfer imaging and artificial intelligence analysis based on MRI images can provide more objective information for the activity staging of TAO from a variety of perspectives. In this paper, we summarized the application of these techniques in the extraocular muscle, orbital fat, lacrimal gland and optic nerve of TAO patients, and combined with the measured parameter values to determine the stage of TAO. It is of great significance to guide clinical decision-making, and is expected to provide reference direction for future research.
[Keywords] thyroid-associated ophthalmopathy;extraocular muscles;clinical activity score;magnetic resonance imaging;functional magnetic resonance imaging;diagnostic imaging;artificial intelligence

ZHANG Yingcong1   BI Qiu2   GONG Xiarong1, 2*   ZHANG Jie2   LI Qingrui1   WANG Qian1   LI Chenrong1   CHENG Changxin1  

1 College of Medicine, Kunming University of Science and Technology, Kunming 650000, China

2 Department of MRI, the First People's Hospital of Yunnan Province (the Affiliated Hospital of Kunming University of Science and Technology), Kunming 650032, China

Corresponding author: Gong XR, E-mail:

Conflicts of interest   None.

ACKNOWLEDGMENTS Yunnan Health Training Project of High Level Talents (No. H-2019070).
Received  2023-04-18
Accepted  2023-09-06
DOI: 10.12015/issn.1674-8034.2023.09.023
ZHANG Y C, BI Q, GONG X R, et al. Research progress of magnetic resonance imaging in the assessment of TAO activity[J]. Chin J Magn Reson Imaging, 2023, 14(9): 125-130. DOI:10.12015/issn.1674-8034.2023.09.023.

BARTALENA L, PIANTANIDA E, GALLO D, et al. Epidemiology, natural history, risk factors, and prevention of Graves' orbitopathy[J/OL]. Front Endocrinol, 2020, 11: 615993 [2023-04-17]. DOI: 10.3389/fendo.2020.615993.
MEN C J, KOSSLER A L, WESTER S T. Updates on the understanding and management of thyroid eye disease[J/OL]. Ther Adv Ophthalmol, 2021, 13: 25158414211027760 [2023-04-17]. DOI: 10.1177/25158414211027760.
BARTALENA L, BALDESCHI L, BOBORIDIS K, et al. The 2016 European thyroid association/european group on Graves' orbitopathy guidelines for the management of Graves' orbitopathy[J]. Eur Thyroid J, 2016, 5(1): 9-26. DOI: 10.1159/000443828.
TACHIBANA S, MURAKAMI T, NOGUCHI H, et al. Orbital magnetic resonance imaging combined with clinical activity score can improve the sensitivity of detection of disease activity and prediction of response to immunosuppressive therapy for Graves' ophthalmopathy[J]. Endocr J, 2010, 57(10): 853-861. DOI: 10.1507/endocrj.k10e-156.
TORTORA F, CIRILLO M, FERRARA M, et al. Disease activity in Graves' ophthalmopathy: diagnosis with orbital MR imaging and correlation with clinical score[J]. Neuroradiol J, 2013, 26(5): 555-564. DOI: 10.1177/197140091302600509.
MAYER E, HERDMAN G, BURNETT C, et al. Serial STIR magnetic resonance imaging correlates with clinical score of activity in thyroid disease[J]. Eye, 2001, 15(Pt 3): 313-318. DOI: 10.1038/eye.2001.102.
GE Q, ZHANG X H, WANG L, et al. Quantitative evaluation of activity of thyroid-associated Ophthalmopathy using short-tau inversion recovery (STIR) sequence[J/OL]. BMC Endocr Disord, 2021, 21(1): 226 [2023-04-17]. DOI: 10.1186/s12902-021-00895-3.
HU H, XU X Q, CHEN L, et al. Predicting the response to glucocorticoid therapy in thyroid-associated ophthalmopathy: mobilizing structural MRI-based quantitative measurements of orbital tissues[J]. Endocrine, 2020, 70(2): 372-379. DOI: 10.1007/s12020-020-02367-5.
HIGASHIYAMA T, IWASA M, OHJI M. Quantitative analysis of inflammation in orbital fat of thyroid-associated ophthalmopathy using MRI signal intensity[J/OL]. Sci Rep, 2017, 7(1): 16874 [2023-04-17]. DOI: 10.1038/s41598-017-17257-6.
HU H, XU X Q, WU F Y, et al. Diagnosis and stage of Graves' ophthalmopathy: efficacy of quantitative measurements of the lacrimal gland based on 3-T magnetic resonance imaging[J]. Exp Ther Med, 2016, 12(2): 725-729. DOI: 10.3892/etm.2016.3389.
MA J F. Dixon techniques for water and fat imaging[J]. J Magn Reson Imaging, 2008, 28(3): 543-558. DOI: 10.1002/jmri.21492.
CHEN L, HU H, CHEN H H, et al. Usefulness of two-point Dixon T2-weighted imaging in thyroid-associated ophthalmopathy: comparison with conventional fat saturation imaging in fat suppression quality and staging performance[J/OL]. Br J Radiol, 2021, 94(1118): 20200884 [2023-04-17]. DOI: 10.1259/bjr.20200884.
OLLITRAULT A, CHARBONNEAU F, HERDAN M L, et al. Dixon-T2WI magnetic resonance imaging at 3tesla outperforms conventional imaging for thyroid eye disease[J]. Eur Radiol, 2021, 31(7): 5198-5205. DOI: 10.1007/s00330-020-07540-y.
LI R C, HUANG X H, FU W H, et al. Clinical value of MR quantitative fat analysis in orbits of patients with Graves ophthalmopathy[J]. J Sun Yat Sen Univ Med Sci, 2019, 40(6): 875-880. DOI: 10.13471/j.cnki.j.sun.yat-sen.univ(med.sci).2019.0121.
FENG X T, LUO Y S, LI Z F, et al. The exploration on clinical value of MRI fat quantification in patients with thyroid associated ophthalmopathy[J]. Chin J Endocrinol Metab, 2020, 36(8): 690-695. DOI: 10.3760/cma.j.cn311282-20200109-00010.
GUO Y, HUO L, WANG P H, et al. Evaluating the microcirculation of normal extraocular muscles using quantitative dynamic contrast-enhanced magnetic resonance imaging[J]. J Comput Assist Tomogr, 2016, 40(3): 419-423. DOI: 10.1097/RCT.0000000000000388.
HUO L, YAN S, WANG J, et al. The value of quantitative dynamic-enhanced MRI in evaluating extra-ocular muscle involvement in patients with chronic thyroid-associated ophthalmopathy[J]. Chin J Magn Reson Imag, 2014, 5(1): 30-34. DOI: 10.3969/j.issn.1674-8034.2014.01.007.
JIANG H, WANG Z C, XIAN J F, et al. Evaluation of rectus extraocular muscles using dynamic contrast-enhanced MR imaging in patients with Graves' ophthalmopathy for assessment of disease activity[J]. Acta Radiol, 2012, 53(1): 87-94. DOI: 10.1258/ar.2011.110431.
LINGAM R K, MUNDADA P, LEE V. Novel use of non-echo-planar diffusion weighted MRI in monitoring disease activity and treatment response in active Grave's orbitopathy: an initial observational cohort study[J]. Orbit, 2018, 37(5): 325-330. DOI: 10.1080/01676830.2017.1423343.
LIU X T, SU Y, JIANG M D, et al. Application of magnetic resonance imaging in the evaluation of disease activity in Graves' ophthalmopathy[J]. Endocr Pract, 2021, 27(3): 198-205. DOI: 10.1016/j.eprac.2020.09.008.
WANG F F, CHENG J L, ZHANG Y, et al. Application of MR high - definition resolution readout segmentation of long variable echo-trains diffusion weighted imaging in the diagnosis of thyroid associated ophthalmopathy[J]. Int Eye Sci, 2020, 20(12): 2129-2133. DOI: 10.3980/j.issn.1672-5123.2020.12.23.
FU Q, LIU D X, MA H, et al. Turbo gradient and spin-echo BLADE-DWI for extraocular muscles in thyroid-associated ophthalmopathy[J/OL]. J Clin Med, 2023, 12(1): 344 [2023-04-17]. DOI: 10.3390/jcm12010344.
RAZEK A A, EL-HADIDY E M, MOAWAD M E, et al. Assessment of lacrimal glands in thyroid eye disease with diffusion-weighted magnetic resonance imaging[J/OL]. Pol J Radiol, 2019, 84: e142-e146 [2023-04-17]. DOI: 10.5114/pjr.2019.84096.
WU Y, LAO Z, ZHANG S, et al. Evaluation of extraocular muscles in patients with thyroid associated ophthalmopathy using apparent diffusion coefficient measured by magnetic resonance imaging before and after radiation therapy[J]. Acta Radiol, 2022, 63(9): 1180-1186. DOI: 10.1177/02841851211034042.
XU X Q, LIU J, HU H, et al. Improve the image quality of orbital 3 T diffusion-weighted magnetic resonance imaging with readout-segmented echo-planar imaging[J]. Clin Imaging, 2016, 40(4): 793-796. DOI: 10.1016/j.clinimag.2016.03.002.
LEE H, LEE Y H, SUH S I, et al. Characterizing intraorbital optic nerve changes on diffusion tensor imaging in thyroid eye disease before dysthyroid optic neuropathy[J]. J Comput Assist Tomogr, 2018, 42(2): 293-298. DOI: 10.1097/RCT.0000000000000680.
ZHANG X H, LI Y M, YU B, et al. The value of high resolution diffusion tensor imaging in evaluating disease activity in patients with thyroid-associated ophthalmopathy[J]. Chin Comput Med Imag, 2021, 27(5): 403-407. DOI: 10.3969/j.issn.1006-5741.2021.05.006.
CAO Y Y, HU H, WU Q, et al. Quantitative measurement of diffusion tensor imaging based on readout-segmented echo-planar imaging of lacrimal glands in evaluating disease activity of thyroid-associated ophthalmopathy[J]. Chin J Med Imag, 2022, 30(5): 447-450. DOI: 10.3969/j.issn.1005-5185.2022.05.006.
CHEN L, HU H, CHEN W, et al. Usefulness of readout-segmented EPI-based diffusion tensor imaging of lacrimal gland for detection and disease staging in thyroid-associated ophthalmopathy[J/OL]. BMC Ophthalmol, 2021, 21(1): 281 [2023-04-17]. DOI: 10.1186/s12886-021-02044-9.
CHEN H H, HU H, CHEN W, et al. Thyroid-associated orbitopathy: evaluating microstructural changes of extraocular muscles and optic nerves using readout-segmented echo-planar imaging-based diffusion tensor imaging[J]. Korean J Radiol, 2020, 21(3): 332-340. DOI: 10.3348/kjr.2019.0053.
ZHANG X H, ZHANG Z W, LÜ F J, et al. The study of high-resolution diffusion tensor imaging in thyroid-associated ophthalmopathy[J]. Chin J Magn Reson Imag, 2021, 12(9): 11-14. DOI: 10.12015/issn.1674-8034.2021.09.003.
HE Y B, XIANG N, SHI S M, et al. The diagnostic value of orbital magnetic resonance imaging T2-Mapping in patients with active Graves' ophthalmopathy[J]. Chin J Endocrinol Metab, 2015, 31(4): 327-332. DOI: 10.3760/cma.j.issn.1000-6699.2015.04.009.
HOU K, AI T, HU W K, et al. Three dimensional orbital magnetic resonance T2-mapping in the evaluation of patients with Graves' ophthalmopathy[J]. Huazhong Keji Daxue Xuebao Yixue Yingdewen Ban, 2017, 37(6): 938-942. DOI: 10.1007/s11596-017-1831-8.
CHEN W, HU H, XU X Q, et al. Clinical value of quantitative measurements of extraocular muscles with T2 mapping in the diagnosis and staging of thyroid-associated ophthalmopathy[J]. Acta Univ Med Nanjing Nat Sci, 2019, 39(1): 141-144. DOI: 10.7655/NYDXBNS20190129.
LUO B, WANG W, LI X Y, et al. Correlation analysis between intraocular pressure and extraocular muscles based on orbital magnetic resonance T2 mapping in thyroid-associated ophthalmopathy patients[J/OL]. J Clin Med, 2022, 11(14): 3981 [2023-04-17]. DOI: 10.3390/jcm11143981.
DAS T, ROOS J C P, PATTERSON A J, et al. T2-relaxation mapping and fat fraction assessment to objectively quantify clinical activity in thyroid eye disease: an initial feasibility study[J]. Eye, 2019, 33(2): 235-243. DOI: 10.1038/s41433-018-0304-z.
WU D D, ZHU H Z, HONG S B, et al. Utility of multi-parametric quantitative magnetic resonance imaging of the lacrimal gland for diagnosing and staging Graves' ophthalmopathy[J/OL]. Eur J Radiol, 2021, 141: 109815 [2023-04-17]. DOI: 10.1016/j.ejrad.2021.109815.
ZHAI L H, LUO B, WU H Y, et al. Prediction of treatment response to intravenous glucocorticoid in patients with thyroid-associated ophthalmopathy using T2 mapping and T2 IDEAL[J/OL]. Eur J Radiol, 2021, 142: 109839 [2023-04-17]. DOI: 10.1016/j.ejrad.2021.109839.
ZHAI L H, WANG Q X, LIU P, et al. T2 mapping with and without fat-suppression to predict treatment response to intravenous glucocorticoid therapy for thyroid-associated ophthalmopathy[J]. Korean J Radiol, 2022, 23(6): 664-673. DOI: 10.3348/kjr.2021.0627.
TENG J, HU H, XU X Q, et al. Preliminary exploration of MR T1-mapping in clinical staging of thyroid-related ophthalmopathy[J]. Radiol Pract, 2021, 36(12): 1499-1502. DOI: 10.13609/j.cnki.1000-0313.2021.12.008.
CHEN L, CHEN W, CHEN H H, et al. Radiological staging of thyroid-associated ophthalmopathy: comparison of T1 mapping with conventional MRI[J/OL]. Int J Endocrinol, 2020, 2020: 2575710 [2023-04-17]. DOI: 10.1155/2020/2575710.
MA R Q, GENG Y, GAN L, et al. Quantitative T1 mapping MRI for the assessment of extraocular muscle fibrosis in thyroid-associated ophthalmopathy[J]. Endocrine, 2022, 75(2): 456-464. DOI: 10.1007/s12020-021-02873-0.
SLED J G. Modelling and interpretation of magnetization transfer imaging in the brain[J/OL]. NeuroImage, 2018, 182: 128-135 [2023-04-17]. DOI: 10.1016/j.neuroimage.2017.11.065.
HU H, CHEN L, ZHOU J, et al. Multiparametric magnetic resonance imaging for differentiating active from inactive thyroid-associated ophthalmopathy: added value from magnetization transfer imaging[J/OL]. Eur J Radiol, 2022, 151: 110295 [2023-04-17]. DOI: 10.1016/j.ejrad.2022.110295.
ZHOU J, XU X Q, HU H, et al. Integrating magnetization transfer imaging and fat suppression T 2WI for predicting the clinical activity of Graves ophthalmopathy[J]. Chin J Radiol, 2022, 56(9): 996-1000. DOI: 10.3760/cma.j.cn112149-20210914-00853.
JIANG W H, HU H, CHEN H H, et al. The value of quantitative parameters on magnetization transfer imaging of lacrimal glands in distinguishing the clinical activity of thyroid-associated ophthalmopathy[J]. Chin J Magn Reson Imag, 2022, 13(11): 17-21. DOI: 10.12015/issn.1674-8034.2022.11.004.
LIN C Y, SONG X F, LI L H, et al. Detection of active and inactive phases of thyroid-associated ophthalmopathy using deep convolutional neural network[J/OL]. BMC Ophthalmol, 2021, 21(1): 39 [2023-04-17]. DOI: 10.1186/s12886-020-01783-5.
HU H, CHEN H H, CHEN W, et al. T2 mapping histogram at extraocular muscles for predicting the response to glucocorticoid therapy in patients with thyroid-associated ophthalmopathy[J/OL]. Clin Radiol, 2021, 76(2): 159.e1-159159.e8 [2023-04-17]. DOI: 10.1016/j.crad.2020.09.005.
LIU P, LUO B, CHEN L, et al. Baseline volumetric T2 relaxation time histogram analysis: can it be used to predict the response to intravenous methylprednisolone therapy in patients with thyroid-associated ophthalmopathy?[J/OL]. Front Endocrinol, 2021, 12: 614536 [2023-04-17]. DOI: 10.3389/fendo.2021.614536.
WU H Y, LUO B, ZHAO Y L, et al. Radiomics analysis of the optic nerve for detecting dysthyroid optic neuropathy, based on water-fat imaging[J/OL]. Insights Imaging, 2022, 13(1): 154 [2023-04-17]. DOI: 10.1186/s13244-022-01292-7.

PREV Implications of habitat imaging-based multisequence MRI in adult-type diffuse glioma
NEXT Application and research progress of extracellular volume based on MRI and CT in malignant tumor

Tel & Fax: +8610-67113815    E-mail: