Skip to main content

Advertisement

Log in

Morphological and microstructural brain changes in thyroid-associated ophthalmopathy: a combined voxel-based morphometry and diffusion tensor imaging study

  • Original Article
  • Published:
Journal of Endocrinological Investigation Aims and scope Submit manuscript

Abstract

Purpose

To explore the morphological and microstructural changes of grey and white matter in the patients of thyroid-associated ophthalmopathy (TAO).

Methods

Twenty-five TAO patients and 25 well-matched healthy controls were recruited. Structural T1- and diffusion-weighted magnetic resonance imaging data were analyzed using voxel-based morphometry and voxel-based analysis of diffusion tensor imaging.

Results

Compared with healthy controls, TAO group showed significantly decreased grey matter volume in the brain region of the right middle frontal gyrus. Meanwhile, TAO group showed significantly decreased fractional anisotropy (FA), but increased mean, axial and radial diffusivities in the brain regions of the right superior occipital gyrus, middle occipital gyrus and cuneus in TAO group. In addition, the FA value in significant brain regions showed a positive correlation with visual acuity (r = 0.456, P = 0.025) and a negative correlation with disease duration (r =  − 0.609, P = 0.003).

Conclusion

Significant morphological and microstructural abnormalities in areas corresponding to known functional deficits of vision and cognition could be found in TAO patients. These results extended our understanding of neural relationships with TAO.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Kilicarslan R, Alkan A, Ilhan MM, Yetis H, Aralasmak A, Tasan E (2015) Graves’ ophthalmopathy: the role of diffusion-weighted imaging in detecting involvement of extraocular muscles in early period of disease. Br J Radiol. https://doi.org/10.1259/bjr.20140677

    Article  PubMed  PubMed Central  Google Scholar 

  2. Li Q, Ye H, Ding Y et al (2017) Clinical characteristics of moderate-to-severe thyroid associated ophthalmopathy in 354 Chinese cases. PLoS ONE. https://doi.org/10.1371/journal.pone.0176064

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bruscolini A, Sacchetti M, La Cava M et al (2018) Quality of life and neuropsychiatric disorders in patients with Graves’ Orbitopathy: Current concepts. AUTOIMMUN REV 17(7):639–643

    Article  PubMed  Google Scholar 

  4. Özkan B, Anik Y, Katre B, Altintaş Ö, Gençtürk M, Yüksel N (2015) Quantitative assessment of optic nerve with diffusion tensor imaging in patients with thyroid orbitopathy. Ophthalmic Plast Reconstr Surg 31(5):391–395

    Article  PubMed  Google Scholar 

  5. Riguetto CM, Neto AM, Tambascia MA, Zantut-Wittmann DE (2019) The relationship between quality of life, cognition, and thyroid status in Graves' disease. Endocrine 63(1):87–93

    Article  CAS  PubMed  Google Scholar 

  6. Bauer M, Goetz T, Glenn T, Whybrow PC (2008) The thyroid-brain interaction in thyroid disorders and mood disorders. J Neuroendocrinol 20(10):1101–1114

    Article  CAS  PubMed  Google Scholar 

  7. Ashburner J, Friston KJ (2000) Voxel-based morphometry–the methods. Neuroimage. https://doi.org/10.1006/nimg.2000.0582

    Article  PubMed  Google Scholar 

  8. Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15(7–8):435–455

    Article  PubMed  Google Scholar 

  9. Amlien IK, Fjell AM (2014) Diffusion tensor imaging of white matter degeneration in Alzheimer's disease and mild cognitive impairment. Neuroscience 276:206–215

    Article  CAS  PubMed  Google Scholar 

  10. Bennett IJ, Madden DJ (2014) Disconnected aging: cerebral white matter integrity and age-related differences in cognition. Neuroscience 276:187–205

    Article  CAS  PubMed  Google Scholar 

  11. Soares JM, Marques P, Alves V, Sousa N (2013) A hitchhiker’s guide to diffusion tensor imaging. Front Neurosci 7:31

    Article  PubMed  PubMed Central  Google Scholar 

  12. Li Q, Jiang Q, Guo M, Li Q, Cai C, Yin X (2013) Grey and white matter changes in children with monocular amblyopia: voxel-based morphometry and diffusion tensor imaging study. Br J Ophthalmol 97(4):524–529

    Article  PubMed  Google Scholar 

  13. Yan X, Lin X, Wang Q et al (2010) Dorsal visual pathway changes in patients with comitant extropia. PLoS ONE 5(6):e10931

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Li C, Cai P, Shi L et al (2012) Voxel-based morphometry of the visual-related cortex in primary open angle glaucoma. Curr Eye Res 37(9):794–802

    Article  PubMed  Google Scholar 

  15. Huang X, Zhang Q, Hu PH et al (2016) White and gray matter volume changes and correlation with visual evoked potential in patients with optic neuritis: a voxel-based morphometry study. Med Sci Monit 22:1115–1123

    Article  PubMed  PubMed Central  Google Scholar 

  16. Silkiss RZ, Wade AR (2016) Neuroanatomic variations in graves’ dysthyroid ophthalmopathy as studied with MRI. Trans Am Ophthalmol Soc 114:T9

    PubMed  Google Scholar 

  17. Bartalena L, Baldeschi L, Boboridis K et al (2016) The 2016 european thyroid association/european group on graves’ orbitopathy guidelines for the management of graves’ orbitopathy. Eur Thyroid J 5(1):9–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Yan CG, Wang XD, Zuo XN, Zang YF (2016) DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics 14(3):339–351

    Article  PubMed  Google Scholar 

  19. Seeley WW, Menon V, Schatzberg AF (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Huang J, Duan Y, Liu S et al (2018) Altered brain structure and functional connectivity of primary visual cortex in optic neuritis. Front Hum Neurosci 12:473

    Article  PubMed  PubMed Central  Google Scholar 

  21. Demet MM, Ozmen B, Deveci A, Boyvada S, Adigüzel H, Aydemir O (2002) Depression and anxiety in hyperthyroidism. Arch Med Res 33(6):552–556

    Article  PubMed  Google Scholar 

  22. Vogel A, Elberling TV, Hording M et al (2007) Affective symptoms and cognitive functions in the acute phase of Graves’ thyrotoxicosis. Psychoneuroendocrino 32(1):36–43

    Article  Google Scholar 

  23. MacCrimmon DJ, Wallace JE, Goldberg WM, Streiner DL (1979) Emotional disturbance and cognitive deficits in hyperthyroidism. Psychosom Med 41(4):331–340

    Article  CAS  PubMed  Google Scholar 

  24. Singh S, Modi S, Bagga D, Kaur P, Shankar LR, Khushu S (2013) Voxel-based morphometric analysis in hypothyroidism using diffeomorphic anatomic registration via an exponentiated lie algebra algorithm approach. J Neuroendocrinol 25(3):229–234

    Article  CAS  PubMed  Google Scholar 

  25. Chen Q, Zheng W, Chen X et al (2018) Whether visual-related structural and functional changes occur in brain of patients with Acute incomplete cervical cord injury: a multimodal based MRI study. Neuroscience 393:284–294

    Article  CAS  PubMed  Google Scholar 

  26. Carlson S, Martinkauppi S, Rama P, Salli E, Korvenoja A, Aronen HJ (1998) Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. Cereb Cortex 8(8):743–752

    Article  CAS  PubMed  Google Scholar 

  27. Sweeney JA, Mintun MA, Kwee S et al (1996) Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J Neurophysiol 75(1):454–468

    Article  CAS  PubMed  Google Scholar 

  28. Ren Z, Zhang Y, He H, Feng Q, Bi T, Qiu J (2019) The different brain mechanisms of object and spatial working memory: voxel-based morphometry and resting-state functional connectivity. Front Hum Neurosci 13:248

    Article  PubMed  PubMed Central  Google Scholar 

  29. Tang X, Liu H, Chen L et al (2018) Semi-automatic volume measurement for orbital fat and total extraocular muscles based on Cube FSE-flex sequence in patients with thyroid-associated ophthalmopathy. Clin Radiol 73(8):711–759

    Article  Google Scholar 

  30. Sykova E (2004) Extrasynaptic volume transmission and diffusion parameters of the extracellular space. Neuroscience 129(4):861–876

    Article  CAS  PubMed  Google Scholar 

  31. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17(3):1429–1436

    Article  PubMed  Google Scholar 

  32. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20(3):1714–1722

    Article  PubMed  Google Scholar 

  33. Bavelier D, Neville HJ (2002) Cross-modal plasticity: where and how? Nat Rev Neurosci 3(6):443–452

    Article  CAS  PubMed  Google Scholar 

  34. Tu S, Qiu J, Martens U, Zhang Q (2013) Category-selective attention modulates unconscious processes in the middle occipital gyrus. Conscious Cogn 22(2):479–485

    Article  PubMed  Google Scholar 

  35. Zhu PW, Huang X, Ye L (2018) Altered intrinsic functional connectivity of the primary visual cortex in youth patients with comitant exotropia: a resting state fMRI study. Int J Ophthalmol 11(4):668–673

    PubMed  PubMed Central  Google Scholar 

  36. Wyble B, Swan G (2015) Mapping the spatiotemporal dynamics of interference between two visual targets. Atten Percept Psychophys 77(7):2331–2343

    Article  PubMed  Google Scholar 

  37. Gerard-Mercier F, Carelli PV, Pananceau M, Troncoso XG, Frégnac Y (2016) Synaptic correlates of low-level perception in V1. J Neurosci 36(14):3925–3942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ouyang J, Yang L, Huang X et al (2017) The atrophy of white and gray matter volume in patients with comitant strabismus: evidence from a voxel-based morphometry study. Mol Med Rep 16(3):3276–3282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lan DY, Zhu PW, He Y et al (2019) Gray matter volume changes in patients with acute eye pain: a voxel-based morphometry study. Transl Vis Sci Technol 8(1):1

    Article  PubMed  PubMed Central  Google Scholar 

  40. Yeatts RP (2005) Quality of life in patients with Graves ophthalmopathy. Trans Am Ophthalmol Soc 103(368):411

    Google Scholar 

Download references

Funding

This work was supported by National Natural Science Foundation of China (NSFC) (81801659 to Hao Hu) and ‘Thyroid Research Program of Young and Middle-aged physicians’ from China Health Promotion Foundation.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: Hao Hu, Xiao-Quan Xu an Fei-Yun Wu; Methodology: Qian Wu, Wen Chen and Lu Chen; Writing—original draft preparation: Qian Wu; Writing—review and editing: Hao Hu, Wen Chen and Xiao-Quan Xu; Funding acquisition: Hao Hu; Resources: Huan-Huan Chen; Supervision: Fei-Yun Wu.

Corresponding authors

Correspondence to X.-Q. Xu or F.-Y. Wu.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

Institutional Review Board approval was obtained.

Informed consent

Informed consents were obtained from all participants.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Q., Hu, H., Chen, W. et al. Morphological and microstructural brain changes in thyroid-associated ophthalmopathy: a combined voxel-based morphometry and diffusion tensor imaging study. J Endocrinol Invest 43, 1591–1598 (2020). https://doi.org/10.1007/s40618-020-01242-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40618-020-01242-4

Keywords

Navigation