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Current status and research progress of MRI for thyroid-associated ophthalmopathy
WANG Yunmeng  CUI Yuanyuan  XIAO Yi 

Cite this article as: WANG Y M, CUI Y Y, XIAO Y. Current status and research progress of MRI for thyroid-associated ophthalmopathy[J]. Chin J Magn Reson Imaging, 2024, 15(1): 205-210, 234. DOI:10.12015/issn.1674-8034.2024.01.035.


[Abstract] Thyroid-associated ophthalmopathy (TAO) is an autoimmune disease which leads the incidence of orbital disease in adults. Clinically, patients with TAO are classified into active and inactive phases mainly based on the clinical activity score (CAS). Determination of TAO activity is critical to the choice of treatment options, however CAS is influenced by clinician experience and patient complaints. Magnetic resonance imaging (MRI) can not only provide anatomical information about the orbital structures, but also allow the analysis of pathological changes in each structure by quantitative evaluation. MRI conventional morphological sequences (T1WI, T2WI), magnetic resonance functional imaging (diffusion-weighted imaging, diffusion tensor imaging), magnetic resonance quantitative techniques (T1 mapping, T2 mapping), chemical shift imaging techniques (Dixion, iterative decomposition of water and fat with echo asymmetry and least-squares estimation quentification sequence), and radiomics play an important role in the activity, severity, complication, and treatment responsiveness of TAO. In this paper, we concluded the application of these techniques to the involved structures (extraocular muscles, optic nerve, lacrimal gland and retro-orbital fat) in patients with TAO. It is expected to suggest the important value of multisequence and multiparameter MRI for the clinical management of TAO and to guide the choice of treatment options in the clinic.
[Keywords] thyroid-related ophthalmopathy；magnetic resonance imaging；dysthyroid optic neuropathy；clinical activity score；assessment of efficacy

WANG Yunmeng1, 2   CUI Yuanyuan1   XIAO Yi2*  

1 Graduate School, Bengbu Medical University, Bengbu 233000, China

2 Department of Radiology, Second Affiliated Hospital of Naval Medical University, Shanghai 200003, China

Corresponding author: XIAO Y, E-mail: xiaoyi@188.com

Conflicts of interest   None.

Received  2023-08-29
Accepted  2024-01-05
DOI: 10.12015/issn.1674-8034.2024.01.035
Cite this article as: WANG Y M, CUI Y Y, XIAO Y. Current status and research progress of MRI for thyroid-associated ophthalmopathy[J]. Chin J Magn Reson Imaging, 2024, 15(1): 205-210, 234. DOI:10.12015/issn.1674-8034.2024.01.035.

[1]
BURCH H B, PERROS P, BEDNARCZUK T, et al. Management of thyroid eye disease: a consensus statement by the American thyroid association and the European thyroid association[J]. Thyroid, 2022, 32(12): 1439-1470. DOI: 10.1089/thy.2022.0251.
[2]
TAYLOR P N, ZHANG L, LEE R W J, et al. New insights into the pathogenesis and nonsurgical management of Graves orbitopathy[J]. Nat Rev Endocrinol, 2020, 16(2): 104-116. DOI: 10.1038/s41574-019-0305-4.
[3]
WANG D D, QIN Q, LI R, et al. Research progresses of imaging methods in diagnosis of thyroid-associated ophthalmopathy[J]. Chin J Med Imag Technol, 2020, 36(11): 1746-1749. DOI: 10.13929/j.issn.1003-3289.2020.11.037.
[4]
SONG C, LUO Y S, YU G F, et al. Current insights of applying MRI in Graves' ophthalmopathy[J/OL]. Front Endocrinol, 2022, 13: 991588 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/36267571/. DOI: 10.3389/fendo.2022.991588.
[5]
ČIVRNÝ J, KARHANOVÁ M, HÜBNEROVÁ P, et al. MRI in the assessment of thyroid-associated orbitopathy activity[J]. Clin Radiol, 2022, 77(12): 925-934. DOI: 10.1016/j.crad.2022.08.124.
[6]
Head and Neck Group, Radiology Branch of Chinese Medical Association. Expert consensus on eye CT and MRI examination and diagnosis[J]. Chin J Radiol, 2017, 51(9): 648-653. DOI: 10.3760/cma.j.issn.1005?1201.2017.09.004.
[7]
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.
[8]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/29203853/. DOI: 10.1038/s41598-017-17257-6.
[9]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/34774035/. DOI: 10.1186/s12902-021-00895-3.
[10]
ZOU M S, WU D D, ZHU H Z, et al. Multiparametric quantitative MRI for the evaluation of dysthyroid optic neuropathy[J]. Eur Radiol, 2022, 32(3): 1931-1938. DOI: 10.1007/s00330-021-08300-2.
[11]
SHEN J, JIANG W, LUO Y S, et al. Establishment of magnetic resonance imaging 3D reconstruction technology of orbital soft tissue and its preliminary application in patients with thyroid-associated ophthalmopathy[J]. Clin Endocrinol, 2018, 88(5): 637-644. DOI: 10.1111/cen.13564.
[12]
ZHANG T, CHEN R X, YE H J, et al. Orbital MRI 3D reconstruction based on volume rendering in evaluating dysthyroid optic neuropathy[J]. Curr Eye Res, 2022, 47(8): 1179-1185. DOI: 10.1080/02713683.2022.2066697.
[13]
CEVIK Y, TAYLAN SEKEROGLU H, OZGEN B, et al. Clinical and radiological findings in patients with newly diagnosed Graves' ophthalmopathy[J]. Int J Endocrinol, 2021, 2021: 5513008. DOI: 10.1155/2021/5513008.
[14]
FEENEY C, LINGAM R K, LEE V, et al. Non-EPI-DWI for detection, disease monitoring, and clinical decision-making in thyroid eye disease[J]. AJNR Am J Neuroradiol, 2020, 41(8): 1466-1472. DOI: 10.3174/ajnr.A6664.
[15]
POLITI L S, GODI C, CAMMARATA G, et al. Magnetic resonance imaging with diffusion-weighted imaging in the evaluation of thyroid-associated orbitopathy: getting below the tip of the iceberg[J]. Eur Radiol, 2014, 24(5): 1118-1126. DOI: 10.1007/s00330-014-3103-3.
[16]
KILICARSLAN R, ALKAN A, ILHAN M M, et al. Graves' ophthalmopathy: the role of diffusion-weighted imaging in detecting involvement of extraocular muscles in early period of disease[J/OL]. Br J Radiol, 2015, 88(1047): 20140677 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/25525866/. DOI: 10.1259/bjr.20140677.
[17]
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.
[18]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/36615144/. DOI: 10.3390/jcm12010344.
[19]
RITCHIE A E, LEE V, FEENEY C, et al. Using nonechoplanar diffusion-weighted MRI to assess treatment response in active Graves orbitopathy: a novel approach with 2 case reports[J/OL]. Ophthalmic Plast Reconstr Surg, 2016, 32(3): e67-e70 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/25141074/. DOI: 10.1097/IOP.0000000000000248.
[20]
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.
[21]
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.
[22]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/34284740/. DOI: 10.1186/s12886-021-02044-9.
[23]
LI R, LI J, WANG Z C. Diffusion tensor imaging technology to quantitatively assess abnormal changes in patients with thyroid-associated ophthalmopathy[J/OL]. Front Hum Neurosci, 2022, 15: 805945 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/35185495/. DOI: 10.3389/fnhum.2021.805945.
[24]
LIU P, LUO B, ZHAI L H, et al. Multi-parametric diffusion tensor imaging of the optic nerve for detection of dysthyroid optic neuropathy in patients with thyroid-associated ophthalmopathy[J/OL]. Front Endocrinol, 2022, 13: 851143 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/35592782/. DOI: 10.3389/fendo.2022.851143.
[25]
LIU P, LUO B, CHEN L, et al. Preliminary diffusion-tensor imaging evidence for trans-synaptic axonal degeneration in dysthyroid optic neuropathy due to thyroid-associated ophthalmopathy[J]. J Magn Reson Imaging, 2023, 57(3): 834-844. DOI: 10.1002/jmri.28352.
[26]
LIU P, LUO B, FENG Y, et al. Aberrant spontaneous brain activity in patients with thyroid-associated ophthalmopathy with and without optic neuropathy: a resting-state functional MRI study[J]. Eur Radiol, 2023, 33(11): 7981-7991. DOI: 10.1007/s00330-023-09829-0.
[27]
LI R, LI J, WANG Z C. Quantitative assessment of the intraorbital segment of the optic nerve in patients with thyroid orbitopathy using diffusion tensor imaging[J]. Acta Radiol, 2023, 64(2): 725-731. DOI: 10.1177/02841851221082419.
[28]
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.
[29]
LI R, LI J, WANG Z C. Thyroid-associated ophthalmopathy: using diffusion tensor imaging to evaluate visual pathway microstructural changes[J/OL]. Front Neurol, 2022, 13: 1025666 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/36408492/. DOI: 10.3389/fneur.2022.1025666.
[30]
FERNANDES J L, ROCHITTE C E. T1 mapping: technique and applications[J]. Magn Reson Imaging Clin N Am, 2015, 23(1): 25-34. DOI: 10.1016/j.mric.2014.08.007.
[31]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/33144856/. DOI: 10.1155/2020/2575710.
[32]
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.
[33]
MATSUZAWA K, IZAWA S, KATO A, et al. Low signal intensities of MRI T1 mapping predict refractory diplopia in Graves' ophthalmopathy[J]. Clin Endocrinol, 2020, 92(6): 536-544. DOI: 10.1111/cen.14178.
[34]
KIM P K, HONG Y J, IM D J, et al. Myocardial T1 and T2 mapping: techniques and clinical applications[J]. Korean J Radiol, 2017, 18(1): 113-131. DOI: 10.3348/kjr.2017.18.1.113.
[35]
CHEN W, HU H, CHEN H H, et al. Utility of T2 mapping in the staging of thyroid-associated ophthalmopathy: efficiency of region of interest selection methods[J]. Acta Radiol, 2020, 61(11): 1512-1519. DOI: 10.1177/0284185120905032.
[36]
HOCH M J, BRUNO M T, SHEPHERD T M. Advanced MRI of the optic nerve[J]. J Neuroophthalmol, 2017, 37(2): 187-196. DOI: 10.1097/WNO.0000000000000511.
[37]
HU H, CHEN H H, CHEN W, et al. Thyroid-associated ophthalmopathy: preliminary study using T2 mapping to characterize intraorbital optic nerve changes before dysthyroid optic neuropathy[J]. Endocr Pract, 2021, 27(3): 191-197. DOI: 10.1016/j.eprac.2020.09.006.
[38]
LI Z, LUO Y, FENG X, et al. Application of Multiparameter Quantitative Magnetic Resonance Imaging in the Evaluation of Graves' Ophthalmopathy[J/OL]. J Magn Reson Imaging, 2023 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/36780178/. DOI: 10.1002/jmri.28642.
[39]
LI D F, WEN W C, LI H B, et al. Clinical study of intravoxel incoherent motion diffusion-weighted imaging and T2 mapping in evaluating the activity of thyroid-associated ophthalmopathy[J]. Chin J Magn Reson Imag, 2021, 12(10): 66-69, 73. DOI: 10.12015/issn.1674-8034.2021.10.015.
[40]
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]. Clinical Radiology, 2021, 76(2): 159.e1-.e8 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/33010933/. DOI: 10.1016/j.crad.2020.09.005.
[41]
LIU P, CHEN L, WANG Q X, et al. Histogram analysis of T2 mapping for detecting early involvement of extraocular muscles in patients with thyroid-associated ophthalmopathy[J/OL]. Sci Rep, 2020, 10(1): 19445 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/33173086/. DOI: 10.1038/s41598-020-76341-6.
[42]
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.
[43]
WANG Y Y, WU Q, CHEN L, et al. Texture analysis of orbital magnetic resonance imaging for monitoring and predicting treatment response to glucocorticoids in patients with thyroid-associated ophthalmopathy[J]. Endocr Connect, 2021, 10(7): 676-684. DOI: 10.1530/EC-21-0162.
[44]
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]. Frontiers in Endocrinology, 2021, 12 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/33716970/. DOI: 10.3389/fendo.2021.614536.
[45]
HUANG K, LIN X X, LUO Y S, et al. Comparative study on the application of Dixon and SPAIR in thyroid-associated ophthalmopathy[J]. Chin J Magn Reson Imag, 2023, 14(8): 51-57. DOI: 10.12015/issn.1674-8034.2023.08.008.
[46]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/33353397/. DOI: 10.1259/bjr.20200884.
[47]
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.
[48]
GAO S, CHEN L, HU H, et al. The value of Dixon in the evaluation of early optic nerve changes in patients with thyroid-associated ophthalmopathy[J]. J Nanjing Med Univ Nat Sci, 2022, 42(4): 556-559, 577. DOI: 10.7655/NYDXBNS20220415.
[49]
WU H Y, LUO B, YUAN G, et al. The diagnostic value of the IDEAL-T2WI sequence in dysthyroid optic neuropathy: a quantitative analysis of the optic nerve and cerebrospinal fluid in the optic nerve sheath[J]. Eur Radiol, 2021, 31(10): 7419-7428. DOI: 10.1007/s00330-021-08030-5.
[50]
SONG C, LUO Y S, HUANG W H, et al. Extraocular muscle volume index at the orbital apex with optic neuritis: a combined parameter for diagnosis of dysthyroid optic neuropathy[J]. Eur Radiol, 2023, 33(12): 9203-9212. DOI: 10.1007/s00330-023-09848-x.
[51]
KAICHI Y, TANITAME K, ITAKURA H, et al. Orbital fat volumetry and water fraction measurements using T2-weighted FSE-IDEAL imaging in patients with thyroid-associated orbitopathy[J]. AJNR Am J Neuroradiol, 2016, 37(11): 2123-2128. DOI: 10.3174/ajnr.A4859.
[52]
ZHAI L, LUO B, WU H, 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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/34252869/. DOI: 10.1016/j.ejrad.2021.109839.
[53]
DURON L, HERAUD A, CHARBONNEAU F, et al. A magnetic resonance imaging radiomics signature to distinguish benign from malignant orbital lesions[J]. Invest Radiol, 2021, 56(3): 173-180. DOI: 10.1097/RLI.0000000000000722.
[54]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/33446163/. DOI: 10.1186/s12886-020-01783-5.
[55]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/36153469/. DOI: 10.1186/s13244-022-01292-7.
[56]
HU H, CHEN L, ZHANG J L, et al. T2-weighted MR imaging-derived radiomics for pretreatment determination of therapeutic response to glucocorticoid in patients with thyroid-associated ophthalmopathy: comparison with semiquantitative evaluation[J]. J Magn Reson Imaging, 2022, 56(3): 862-872. DOI: 10.1002/jmri.28088.
[57]
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 [2023-09-01]. https://pubmed.ncbi.nlm.nih.gov/35405579/. DOI: 10.1016/j.ejrad.2022.110295.

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