Abstract
Purpose
To compare the electrophysiology between mild thyroid-associated ophthalmopathy (TAO) patients and normal population.
Methods
The present research was a retrospective observational study and enrolled consecutive patients diagnosed with mild TAO according to European Group on Graves’s Orbitopathy with corrected to normal vision. Full-field electroretinography, pattern visual evoked potential (PVEP) and isolated-check visual evoked potential (icVEP) were performed for TAO patients and age-matched normal subjects.
Results
Thirty-two eyes with mild TAO and forty-six eyes from normal subjects were included. Statistically significant increase in the amplitude of dark-adapted 0.01, 3 and 10 ERG and total oscillatory potentials and light-adapted 3 and 30 Hz flicker ERG were observed in TAO patients compared with the normal subjects, but not the latency. No significant difference was observed in the P100 amplitude or latency in 1° and 15′ PVEP between TAO patients and normal subjects. The signal-to-noise ratio (SNR) was not significantly different in TAO patients at the contrast of 1%, 2%, 8%, 16% or 32% icVEP, and the SNR in contrast 4% icVEP was significantly smaller in TAO patients compared to normal subjects.
Conclusion
Mild TAO patients can have electrophysiological changes that might indicate neural changes in the early disease phase.
Similar content being viewed by others
Data availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Chavis PS (2002) Thyroid and the eye. Curr Opin Ophthalmol 13(6):352–356
Menconi F, Marcocci C, Marino M (2014) Diagnosis and classification of Graves’ disease. Autoimmun Rev 13(4–5):398–402. https://doi.org/10.1016/j.autrev.2014.01.013
Garrity JA, Bahn RS (2006) Pathogenesis of graves ophthalmopathy: implications for prediction, prevention, and treatment. Am J Ophthalmol 142(1):147–153. https://doi.org/10.1016/j.ajo.2006.02.047
Anderson RL, Tweeten JP, Patrinely JR, Garland PE, Thiese SM (1989) Dysthyroid optic neuropathy without extraocular muscle involvement. Ophthal Surg 20(8):568–574
Carter KD, Frueh BR, Hessburg TP, Musch DC (1991) Long-term efficacy of orbital decompression for compressive optic neuropathy of Graves’ eye disease. Ophthalmology 98(9):1435–1442
Trobe JD (1981) Optic nerve involvement in dysthyroidism. Ophthalmology 88(6):488–492
Wei YH, Chi MC, Liao SL (2011) Predictability of visual function and nerve fiber layer thickness by cross-sectional areas of extraocular muscles in graves ophthalmopathy. Am J Ophthalmol 151(5):901–906.e901. https://doi.org/10.1016/j.ajo.2010.11.001
Sayin O, Yeter V, Ariturk N (2016) Optic disc, macula, and retinal nerve fiber layer measurements obtained by OCT in thyroid-associated ophthalmopathy. J Ophthalmol 2016:9452687. https://doi.org/10.1155/2016/9452687
Blum Meirovitch S, Leibovitch I, Kesler A, Varssano D, Rosenblatt A, Neudorfer M (2017) Retina and nerve fiber layer thickness in eyes with thyroid-associated ophthalmopathy. Israel Med Assoc J IMAJ 19(5):277–281
Hood DC, Odel JG, Winn BJ (2003) The multifocal visual evoked potential. J Neuro-ophthalmol Off J N Am Neuro-Ophthalmol Soc 23(4):279–289
Holder GE (1997) The pattern electroretinogram in anterior visual pathway dysfunction and its relationship to the pattern visual evoked potential: a personal clinical review of 743 eyes. Eye (London, England) 11(Pt 6):924–934. https://doi.org/10.1038/eye.1997.231
Brecelj J (2003) From immature to mature pattern ERG and VEP. Doc Ophthalmol Adv Ophthalmol 107(3):215–224
Pihl-Jensen G, Schmidt MF, Frederiksen JL (2017) Multifocal visual evoked potentials in optic neuritis and multiple sclerosis: a review. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 128(7):1234–1245. https://doi.org/10.1016/j.clinph.2017.03.047
Parisi V, Miglior S, Manni G, Centofanti M, Bucci MG (2006) Clinical ability of pattern electroretinograms and visual evoked potentials in detecting visual dysfunction in ocular hypertension and glaucoma. Ophthalmology 113(2):216–228. https://doi.org/10.1016/j.ophtha.2005.10.044
Tzekov R, Arden GB (1999) The electroretinogram in diabetic retinopathy. Surv Ophthalmol 44(1):53–60. https://doi.org/10.1016/s0039-6257(99)00063-6
Senger C, Moreto R, Watanabe SES, Matos AG, Paula JS (2020) Electrophysiology in Glaucoma. J Glaucoma 29(2):147–153. https://doi.org/10.1097/ijg.0000000000001422
Spadea L, Bianco G, Dragani T, Balestrazzi E (1997) Early detection of P-VEP and PERG changes in ophthalmic Graves’ disease. Graefe’s Arch Clin Exp Ophthalmol Albrecht von Graefes Archiv fur klinische und Exp Ophthalmol 235(8):501–505
Acaroglu G, Simsek T, Ozalp S, Mutluay A (2003) Subclinical optic neuropathy in Graves’ orbitopathy. Jpn J Ophthalmol 47(5):459–462
Perez-Rico C, Rodriguez-Gonzalez N, Arevalo-Serrano J, Blanco R (2012) Evaluation of multifocal visual evoked potentials in patients with Graves’ orbitopathy and subclinical optic nerve involvement. Doc Ophthalmol Adv Ophthalmol 125(1):11–19. https://doi.org/10.1007/s10633-012-9325-2
Barrio-Barrio J, Sabater AL, Bonet-Farriol E, Velázquez-Villoria Á, Galofré JC (2015) Graves’ ophthalmopathy: VISA versus EUGOGO classification, assessment, and management. J Ophthalmol 2015:249125. https://doi.org/10.1155/2015/249125
McCulloch DL, Marmor MF, Brigell MG, Hamilton R, Holder GE, Tzekov R, Bach M (2015) ISCEV standard for full-field clinical electroretinography (2015 update). Doc Ophthalmol Adv Ophthalmol 130(1):1–12. https://doi.org/10.1007/s10633-014-9473-7
Odom JV, Bach M, Brigell M, Holder GE, McCulloch DL, Mizota A, Tormene AP (2016) ISCEV standard for clinical visual evoked potentials: (2016 update). Doc Ophthalmol Adv Ophthalmol 133(1):1–9. https://doi.org/10.1007/s10633-016-9553-y
Bartalena L, Pinchera A, Marcocci C (2000) Management of Graves’ ophthalmopathy: reality and perspectives. Endocr Rev 21(2):168–199. https://doi.org/10.1210/edrv.21.2.0393
Ford BA, Artes PH, McCormick TA, Nicolela MT, LeBlanc RP, Chauhan BC (2003) Comparison of data analysis tools for detection of glaucoma with the Heidelberg Retina Tomograph. Ophthalmology 110(6):1145–1150. https://doi.org/10.1016/s0161-6420(03)00230-6
Sakata LM, Deleon-Ortega J, Sakata V, Girkin CA (2009) Optical coherence tomography of the retina and optic nerve—a review. Clin Exp Ophthalmol 37(1):90–99. https://doi.org/10.1111/j.1442-9071.2009.02015.x
Sen E, Berker D, Elgin U, Tutuncu Y, Ozturk F, Guler S (2012) Comparison of optic disc topography in the cases with graves disease and healthy controls. J Glaucoma 21(9):586–589. https://doi.org/10.1097/ijg.0b013e31822e8c4f
Beden U, Kaya S, Yeter V, Erkan D (2013) Contrast sensitivity of thyroid associated ophthalmopathy patients without obvious optic neuropathy. TheScientificWorldJournal 2013:943789. https://doi.org/10.1155/2013/943789
Kennerdell JS, Rosenbaum AE, El-Hoshy MH (1981) Apical optic nerve compression of dysthyroid optic neuropathy on computed tomography. Arch Ophthalmol (Chicago, Ill:1960) 99(5):807–809
Holder GE, Robson AG, Hogg CR, Kurz-Levin M, Lois N, Bird AC (2003) Pattern ERG: clinical overview, and some observations on associated fundus autofluorescence imaging in inherited maculopathy. Doc Ophthalmol Adv Ophthalmol 106(1):17–23
Weik R, Ruprecht KW (1995) Value of electrophysiology in ophthalmologic monitoring of patients with endocrine orbitopathy. Klin Monatsblatter fur Augenheilkd 206(6):446–450. https://doi.org/10.1055/s-2008-1035485
Tsang SH, Sharma T (2018) Electroretinography. Adv Exp Med Biol 1085:17–20. https://doi.org/10.1007/978-3-319-95046-4_5
Nassr MA, Morris CL, Netland PA, Karcioglu ZA (2009) Intraocular pressure change in orbital disease. Surv Ophthalmol 54(5):519–544. https://doi.org/10.1016/j.survophthal.2009.02.023
Cross JM, Girkin CA, Owsley C, McGwin G Jr (2008) The association between thyroid problems and glaucoma. Br J Ophthalmol 92(11):1503–1505. https://doi.org/10.1136/bjo.2008.147165
Ohtsuka K, Nakamura Y (2000) Open-angle glaucoma associated with Graves disease. Am J Ophthalmol 129(5):613–617
Forte R, Bonavolonta P, Vassallo P (2010) Evaluation of retinal nerve fiber layer with optic nerve tracking optical coherence tomography in thyroid-associated orbitopathy. Ophthalmol J Int d’ophtalmol Int J Ophthalmol Z Augenheilkd 224(2):116–121. https://doi.org/10.1159/000235925
Xu LJ, Zhang L, Li SL, Zemon V, Virgili G, Liang YB (2017) Accuracy of isolated-check visual evoked potential technique for diagnosing primary open-angle glaucoma. Doc Ophthalmol Adv Ophthalmol 135(2):107–119. https://doi.org/10.1007/s10633-017-9598-6
Skottun BC (2016) A few words on differentiating magno- and parvocellular contributions to vision on the basis of temporal frequency. Neurosci Biobehav Rev 71:756–760. https://doi.org/10.1016/j.neubiorev.2016.10.016
Funding
This work was supported by the grant from Chinese Capital’s Funds for Health Improvement and Research (Grant Number: CFH2018-2-4093) and National Science and Technology Major Project (Grant Number: 2018ZX10101004). The sponsor or funding organization had no role in the design or conduct of this research.
Author information
Authors and Affiliations
Contributions
All authors contributed to the conceptualization and design of the research. Data collection was performed by YT, YW and JM, and data analysis was performed by YW, JM and XL. The original draft was written by YW, and the manuscript was reviewed and revised by all authors. All authors approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
The research was conducted according to the principles of the Declaration of Helsinki. And the protocol was approved by the local review board.
Consent for publication
The consent for publication has been obtained from all authors.
Statement of human rights
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.
Statement on the welfare of animals
Not applicable.
Informed consent
Informed consent was not obtained from each individual participant. The ethics committee approved the exemption of informed consent because the research retrospectively collected data and could not obtain consent from each individual participant technically.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Tian, Y., Wang, Y., Ma, J. et al. Application of electrophysiological tests in the evaluation of early thyroid-associated ophthalmopathy. Doc Ophthalmol 142, 343–351 (2021). https://doi.org/10.1007/s10633-020-09808-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10633-020-09808-6