Changes of corneal nerve fiber and the correlation analysis with visual acuity in demyelinating optical neuritis patients_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhao Rui , Wang Leying , Chen Chunli , Zhang Jing , Guo Sitong , Chen Fei , Liu Hongjuan ,  Jiang Libin

Beijing Tongren Hospital Affiliated to Capital Medical University, Beijing 100730, China;

Corresponding author：

Jiang Libin, Email: jlbjlb@sina.com

Keywords：

Demyelinating optic neuritis; Corneal nerve fiber; Aguaporin-4; Myelin oligodendrocyte glycoprotein; In vivo confocal microscopy

DOI：

10.3760/cma.j.cn511434-20221206-00641

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Objective To investigate the changes in the nerve fiber layer of the cornea in patients with demyelinating optic neuritis (DON) and its correlation with visual acuity. Methods A cross-sectional study. From March 2021 to July 2022, 27 cases (39 eyes) of DON patients diagnosed in the Department of Neurology and Ophthalmology of Beijing Tongren Hospital Affiliated to Capital Medical University were enrolled in this study. According to the serological test results, the patients were divided into aquaporin 4 antibody associated optic neuritis (AQP4-ON group) and myelin oligodendrocyte glycoprotein antibody associated optic neuritis (MOG-ON group), with 15 cases (19 eyes) and 12 cases (20 eyes) respectively. According to previous history of glucocorticoid treatment, the patients were divided into glucocorticoid treated group and non-glucocorticoid treated group, with 17 cases (27 eyes) and 10 cases (12 eyes) respectively. Twenty healthy volunteers (20 eyes) with age- and gender-matched were selected as the control group. All eyes underwent best corrected visual acuity (BCVA) and in vivo confocal microscopy (IVCM) examinations. BCVA was performed using Snellen's standard logarithmic visual acuity chart, which was converted into logarithmic minimum angle resolution (logMAR) visual acuity during statistics. The corneal nerve fiber length (CNFL), corneal nerve fiber density (CNFD), corneal nerve fiber branch length (CNBL), corneal nerve fiber branch density (CNBD) and the density of corneal dendritic cells (DC) were detected by IVCM examination. Parameter comparison between groups by t-test and Kruskal-Wallis rank sum test. The correlation between logMAR BCVA and pamameters of corneal nerve fibers were analyzed using Spearman analysis. Results The CNFL, CNFD, and CNBL of the DON group and the control group were (10.67±2.55) mm/mm², (57.78±12.35) root/mm², (3.27±1.34) mm/mm², and (13.74±3.05) mm/mm², (70.95±13.14) root/mm², and (4.22±1.03) mm/mm², respectively; the difference in CNFL, CNFD, and CNBL between the two groups were statistically significant (t=4.089, 3.795, 2.773; P＜0.05). The CNFL, CNBL, and CNBD of the affected eyes in the MOG-ON group and AQP4-ON group were (12.02±2.13) mm/mm², (3.80±1.19) mm/mm², (47.97±8.86) fibers/mm², and (9.25±2.19) mm/mm², (2.72±1.19) mm/mm², (39.43±13.86) fibers/mm², respectively; the differences in CNFL, CNBL, and CNBD between the two groups were statistically significant (t=－4.002, －2.706, －2.306; P＜0.05). The corneal DC density of the patients in the hormone treated group and the non-hormone treated group was (24.43±8.32) and (41.22±9.86) cells/mm², respectively. The difference in corneal DC density between the two subgroups was statistically significant (P＜0.001). Correlation analysis showed that there was a significant negative correlation between logMAR BCVA and CNBL and CNFL in patients with DON (r=－0.422, －0.456; P＜0.05). Conclusions There are different degrees of corneal nerve fiber damage in patients with different types of DON. There was a negative correlation between BCVA and the length of corneal nerve fibers.

Citation： Zhao Rui, Wang Leying, Chen Chunli, Zhang Jing, Guo Sitong, Chen Fei, Liu Hongjuan, Jiang Libin. Changes of corneal nerve fiber and the correlation analysis with visual acuity in demyelinating optical neuritis patients. Chinese Journal of Ocular Fundus Diseases, 2023, 39(4): 312-317. doi: 10.3760/cma.j.cn511434-20221206-00641 Copy

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15.	Labetoulle M, Baudouin C, Calonge M, et al. Role of corneal nerves in ocular surface homeostasis and disease[J]. Acta Ophthalmol, 2019, 97(2): 137-145. DOI: 10.1111/aos.13844.
16.	Bitirgen G, Tinkir KE, Satirtav G, et al. In vivo confocal microscopic evaluation of corneal nerve fibers and dendritic cells in patients with Behçet's disease[J]. Front Neurol, 2018, 9: 204. DOI: 10.3389/fneur.2018.00204.
17.	Cruzat A, Witkin D, Baniasadi N, et al. Inflammation and the nervous system: the connection in the cornea in patients with infectious keratitis[J]. Invest Ophthalmol Vis Sci, 2011, 52(8): 5136-5143. DOI: 10.1167/iovs.10-7048.
18.	Kim S, Park J, Kwon BS, et al. Radiculopathy in neuromyelitis optica. How does anti-AQP4 Ab involve PNS?[J]. Mult Scler Relat Disord, 2017, 18: 77-81. DOI: 10.1016/j.msard.2017.09.006.
19.	Kitada M, Suzuki H, Ichihashi J, et al. Acute combined central and peripheral demyelination showing anti-aquaporin 4 antibody positivity[J]. Intern Med, 2012, 51(17): 2443-2447. DOI: 10.2169/internalmedicine.51.7590.
20.	Nakamura T, Kaneko K, Watanabe G, et al. Myelin oligodendrocyte glycoprotein- IgG-positive, steroid-responsive combined central and peripheral demyelination with recurrent peripheral neuropathy[J]. Neurol Sci, 2021, 42(3): 1135-1138. DOI: 10.1007/s10072-020-04822-7.

1. Ferrari G, Nallasamy N, Downs H, et al. Corneal innervation as a window to peripheral neuropathies[J]. Exp Eye Res, 2013, 113: 148-150. DOI: 10.1016/j.exer.2013.05.016.
2. Fernandes D, Luís M, Cardigos J, et al. Corneal subbasal nerve plexus evaluation by in vivo confocal microscopy in multiple sclerosis: a potential new biomarker[J]. Curr Eye Res, 2021, 46(10): 1452-1459. DOI: 10.1080/02713683.2021.1904509.
3. Petropoulos IN, Kamran S, Li Y, et al. Corneal confocal microscopy: an imaging endpoint for axonal degeneration in multiple sclerosis[J]. Invest Ophthalmol Vis Sci, 2017, 58(9): 3677-3681. DOI: 10.1167/iovs.17-22050.
4. Ferrari G, Grisan E, Scarpa F, et al. Corneal confocal microscopy reveals trigeminal small sensory fiber neuropathy in amyotrophic lateral sclerosis[J]. Front Aging Neurosci, 2014, 6: 278. DOI: 10.3389/fnagi.2014.00278.
5. Gad H, Petropoulos IN, Khan A, et al. Corneal confocal microscopy for the diagnosis of diabetic peripheral neuropathy: a systematic review and meta-analysis[J]. J Diabetes Investig, 2022, 13(1): 134-137. DOI: 10.1111/jdi.13643.
6. Che NN, Jiang QH, Ding GX, et al. Corneal nerve fiber loss relates to cognitive impairment in patients with Parkinson's disease[J]. NPJ Parkinsons Dis, 2021, 7(1): 80. DOI: 10.1038/s41531-021-00225-3.
7. Altıntaş A, Yildiz-Tas A, Yilmaz S, et al. A novel investigation method for axonal damage in neuromyelitis optica spectrum disorder: in vivo corneal confocal microscopy[J/OL]. Mult Scler J Exp Transl Clin, 2021, 7: 2055217321998060[2021-03-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7985945/. DOI:10.1177/2055217321998060.
8. Bitirgen G, Akpinar Z, Malik RA, et al. Use of corneal confocal microscopy to detect corneal nerve loss and increased dendritic cells in patients with multiple sclerosis[J]. JAMA Ophthalmol, 2017, 135(7): 777-782. DOI: 10.1001/jamaophthalmol.2017.1590.
9. Mikolajczak J, Zimmermann H, Kheirkhah A, et al. Patients with multiple sclerosis demonstrate reduced subbasal corneal nerve fibre density[J]. Mult Scler, 2017, 23(14): 1847-1853. DOI: 10.1177/1352458516677590.
10. 中华医学会眼科学分会神经眼科学组, 兰州大学循证医学中心/世界卫生组织指南实施与知识转化合作中心. 中国脱髓鞘性视神经炎诊断和治疗循证指南(2021年)[J]. 中华眼科杂志, 2021, 57(3): 171-186. DOI: 10.3760/cma.j.cn112142-20201124-00769.Neuro-ophthalmology Group of Ophthalmology Branch of Chinese Medical Association, Evidence-based Medicine Center of Lanzhou University/World Health Organization Collaborating Centre for Guideline Implementation and Knowledge Translation. Evidence-based guidelines for diagnosis and treatment of demyelinating optic neuritis in China(2021)[J]. Chin J Ophthalmol, 2021, 57(3): 171-186. DOI: 10.3760/cma.j.cn112142-20201124-00769.
11. 中华医学会眼科学分会神经眼科学组. 视神经炎诊断和治疗专家共识(2014年)[J]. 中华眼科杂志, 2014, 50(6): 459-463. DOI: 10.3760/cma.j.issn.0412-4081.2014.06.013.Neuro-ophthalmology Group, Ophthalmological Branch, Chinese Medical Association. Expert consensus on diagnosis and treatment of optic neuritis (2014)[J]. Chin J Ophthalmol, 2014, 50(6): 459-463. DOI: 10.3760/cma.j.issn.0412-4081.2014.06.013.
12. Moussa G, Bassilious K, Mathews N. A novel excel sheet conversion tool from Snellen fraction to logMAR including 'counting fingers', 'hand movement', 'light perception' and 'no light perception' and focused review of literature of low visual acuity reference values[J]. Acta Ophthalmol, 2021, 99(6): 963-965. DOI: 10.1111/aos.14659.
13. Petzold A, Fraser CL, Abegg M, et al. Diagnosis and classification of optic neuritis[J]. Lancet Neurol, 2022, 21(12): 1120-1134. DOI: 10.1016/S1474-4422(22)00200-9.
14. Liu Y, Chou Y, Dong X, et al. Corneal subbasal nerve analysis using in vivo confocal microscopy in patients with dry eye: analysis and clinical correlations[J]. Cornea, 2019, 38(10): 1253-1258. DOI: 10.1097/ICO.0000000000002060.
15. Labetoulle M, Baudouin C, Calonge M, et al. Role of corneal nerves in ocular surface homeostasis and disease[J]. Acta Ophthalmol, 2019, 97(2): 137-145. DOI: 10.1111/aos.13844.
16. Bitirgen G, Tinkir KE, Satirtav G, et al. In vivo confocal microscopic evaluation of corneal nerve fibers and dendritic cells in patients with Behçet's disease[J]. Front Neurol, 2018, 9: 204. DOI: 10.3389/fneur.2018.00204.
17. Cruzat A, Witkin D, Baniasadi N, et al. Inflammation and the nervous system: the connection in the cornea in patients with infectious keratitis[J]. Invest Ophthalmol Vis Sci, 2011, 52(8): 5136-5143. DOI: 10.1167/iovs.10-7048.
18. Kim S, Park J, Kwon BS, et al. Radiculopathy in neuromyelitis optica. How does anti-AQP4 Ab involve PNS?[J]. Mult Scler Relat Disord, 2017, 18: 77-81. DOI: 10.1016/j.msard.2017.09.006.
19. Kitada M, Suzuki H, Ichihashi J, et al. Acute combined central and peripheral demyelination showing anti-aquaporin 4 antibody positivity[J]. Intern Med, 2012, 51(17): 2443-2447. DOI: 10.2169/internalmedicine.51.7590.
20. Nakamura T, Kaneko K, Watanabe G, et al. Myelin oligodendrocyte glycoprotein- IgG-positive, steroid-responsive combined central and peripheral demyelination with recurrent peripheral neuropathy[J]. Neurol Sci, 2021, 42(3): 1135-1138. DOI: 10.1007/s10072-020-04822-7.

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