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Journal of Peking University (Health Sciences) ›› 2022, Vol. 54 ›› Issue (4): 705-711. doi: 10.19723/j.issn.1671-167X.2022.04.020

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Evaluation of ocular surface status and function in primary Sjögren's syndrome with hypothyroidism

Hao-zhe YU1,Wei-zhen ZENG1,Wen-yu WU1,Zhong-qiang YAO2,*(),Yun FENG1,*()   

  1. 1. Department of Ophthalmology, Peking University Third Hospital, Beijing 100191, China
    2. Department of Rheumatology and Immunology, Peking University Third Hospital, Beijing 100191, China
  • Received:2021-08-16 Online:2022-08-18 Published:2022-08-11
  • Contact: Zhong-qiang YAO,Yun FENG E-mail:yaozhongqiang@sina.com;fengyun@bjmu.edu.cn
  • Supported by:
    the National Nature Science Foundation of China(81700799);the National Nature Science Foundation of China(82070926)

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Abstract:

Objective: To explore the effect of hypothyroidism (HT) on the ocular surface status of patients with primary Sjögren's syndrome-related dry eye (pSS-DED). Methods: The cross-sectional study included 36 patients with pSS-DED who were treated at the dry eye clinic of Peking University Third Hospital from December 2020 to June 2021, of whom 12 were pSS-DED patients combined with HT. In the same period, 24 patients with simple dry eye disease (DED) were served as a control group. All the patients filled out the Ocular Surface Disease Index (OSDI) questionnaire, and performed tear film break-up time (BUT), Schirmer test, tear meniscus height, corneal/conjunctival fluorescein staining, meibomian gland secretion capacity, meibum evaluation and confocal microscope examination. Results: (1) Compared with pSS-DED and simple DED patients, pSS-DED +HT patients had lower average BUT [(2.7±0.8) s], Schirmer test [(4.9±4.8) mm] and tear meniscus height [(0.13±0.03) mm], and the difference was statistically significant (F=12.43, P < 0.01; F=6.96, P < 0.01; F=3.31, P < 0.05). (2) Compared with DED and pSS-DED patients, the meibomian gland secretion capacity and meibomian trait scores of pSS-DED+HT patients were mainly distributed in the high division. There were statistically significant differences in the distribution of secretion capacity of meibomian glands (χ2=10.72, P < 0.05) and meibomian trait assessment scores (χ2=8.34, P < 0.05) among the three groups. (3) Serum total thyroxine and serum free thyroxine levels in the pSS-DED+HT patients showed positive correlation (P < 0.05, P < 0.05) with their BUT (r=0.60, 0.60), Schirmer's test (r=0.64, 0.66) and tear river height (r=0.61, 0.62), independent of lid gland secretory capacity; no significant correlation was found between thyroid-stimulating hormone, anti-thyroglobulin antibody and lid gland secretory capacity. Thyroid hormone, anti-thyroglobulin antibody, and thyroid peroxidase antibody were not found to be significantly correlated with ocular surface status. (4) Compared with pSS-DED, the fiber density of the subbasal nerve plexus in pSS-DED+HT group decreased (t=2.06, P < 0.05), and the curvature score increased (t=2.13, P < 0.05). Conclusion: The ocular surface condition of pSS-DED patients with HT is worse than that of pSS-DED and DED patients. The main manifestations are that tear secretion, tear film stability, secretory function of the meibomian glands, meibum trait and fiber density of the subbasal nerve plexus decrease while the curvature increases. The mechanism might be related to the decrease in thyroid hormone production.

Key words: Primary Sjögren's syndrome, Dry eye disease, Hypothyroidism, Ocular surface status, Primary Sjögren's syndrome dry eye disease

CLC Number: 

  • R593.2

Figure 1

Ocular surface and tear examination results of DED, pSS-DED and pSS-DED with HT patients A, BUT (tear break-up time); B, Schirmer test; C, TMH (tear meniscus height); D, corneal/conjunctival fluorescein staining; E, OSDI (ocular surface disease index). a, DED (dry eye disease); b, pSS (primary Sjögren's syndrome)+DED; c, pSS+DED+HT(hypothyroidism). *P < 0.05; # P < 0.01."

Figure 2

Infrared imaging of meibomian gland morphology A, DED (dry eye disease); B, pSS (primary Sjögren's syndrome)+DED; C, pSS+DED+HT (hypothyroidism)."

Table 1

Spearman's rank correlation analysis of thyroid function indicators and ocular surface status in patients with pSS-DED+HT"

Indicators Value BUT Schirmer TMH Meibomian gland secretion capacity
r P r P r P r P
TT4 4.6±3.8 0.60 P < 0.05 0.64 P < 0.05 0.61 P < 0.05 -0.11 P=0.73
FT4 0.8±0.5 0.60 P < 0.05 0.66 P < 0.05 0.62 P < 0.05 -0.09 P=0.79
TSH 5.2±2.8 -0.51 P=0.09 -0.53 P=0.08 -0.56 P=0.06 0.07 P=0.83
TGAb - -0.20 P=0.52 -0.04 P=0.90 -0.42 P=0.17 -0.49 P=0.11
TPOAb - 0.01 P=0.96 0.48 P=0.11 0.28 P=0.37 -0.48 P=0.12

Figure 3

Confocal microscopical observation Primary Sjögren's syndrome related dry eye disease (pSS-DED) patients: A, corneal epithelial pterygium cells; B, corneal subepithelial nerve; C, corneal stromal cells; D, corneal endothelial cell. pSS-DED+HT (hypothyroidism) patients: E, corneal epithelial pterygium cells; F, corneal subepithelial nerve; G, corneal stromal cells; H, corneal endothelial cell."

Table 2

Dendritic cell density and characteristics of corneal sub-basal nerve plexus in patients with pSS-DED and pSS-DED+HT"

Group Dendritic cell density/mm2 Nerve fiber density/mm2 Nerve fiber length/(mm/mm2) Curvature score
pSS-DED 51.5±9.5 27.3±4.3 12.3±4.1 3.4±0.9
pSS-DED+HT 58.9±18.7 24.5±2.9 10.1±2.9 4.0±0.8
Statistics t=1.30，P=0.21
Cohen’s d=0.50		 t=2.06，P < 0.05
Cohen’s d=0.76		 t=1.62，P=0.11
Cohen’s d=0.62		 t=2.13，P < 0.05
Cohen’s d=0.70
1 Chowdhury F, Tappuni A, Bombardieri M. Biological therapy in primary Sjögren's syndrome: Effect on salivary gland function and inflammation[J/OL]. Front Med, 2021, 8: 707104[2021-07-01]. https://www.frontiersin.org/articles/10.3389/fmed.2021.707104/full.
2 Bron AJ , de Paiva CS , Chauhan SK , et al. TFOS DEWS Ⅱ pathophysiology report[J]. Ocul Surf, 2017, 15 (3): 438- 510.
3 Villarreal-Gonzalez AJ , Rivera-Alvarado IJ , Rodriguez-Gutierrez LA , et al. Analysis of ocular surface damage and visual impact in patients with primary and secondary Sjögren syndrome[J]. Rheumatol Int, 2020, 40 (8): 1249- 1257.
doi: 10.1007/s00296-020-04568-7
4 Xu D , Zhao S , Li Q , et al. Characteristics of Chinese patients with primary Sjögren's syndrome: Preliminary report of a multi-centre registration study[J]. Lupus, 2020, 29 (1): 45- 51.
doi: 10.1177/0961203319889666
5 Wang TJ , Wang IJ , Hu CC , et al. Comorbidities of dry eye disease: A nationwide population-based study[J]. Acta Ophthalmol, 2012, 90 (7): 663- 668.
doi: 10.1111/j.1755-3768.2010.01993.x
6 亚洲干眼协会中国分会, 海峡两岸医药卫生交流协会眼科学专业委员会眼表与泪液病学组中国医师协会眼科医师分会眼表与干眼学组. 中国干眼专家共识: 检查和诊断(2020年)[J]. 中华眼科杂志, 2020, 56 (10): 741- 747.
doi: 10.3760/cma.j.cn112142-20200714-00477
7 Shiboski CH , Shiboski SC , Seror R , et al. 2016 American College of Rheumatology/European League Against Rheumatism Classification Criteria for primary Sjögren's syndrome: A consensus and data-driven methodology involving three international patient cohorts[J]. Arthritis Rheumatol, 2017, 69 (1): 35- 45.
doi: 10.1002/art.39859
8 中华医学会内分泌学分会. 成人甲状腺功能减退症诊治指南[J]. 中华内分泌代谢杂志, 2017, 33 (2): 167- 180.
doi: 10.3760/cma.j.issn.1000-6699.2017.02.018
9 Oliveira-Soto L , Efron N . Morphology of corneal nerves using confocal microscopy[J]. Cornea, 2001, 20 (4): 374- 384.
doi: 10.1097/00003226-200105000-00008
10 Sun X, Lu L, Li Y, et al. Increased risk of thyroid disease in patients with Sjögren's syndrome: A systematic review and meta-analysis[J/OL]. Peerj, 2019, 7: 6737[2021-07-01]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6430100/.
11 Sepulveda JIR , Kvarnstrom M , Eriksson P , et al. Long-term follow-up in primary Sjögren's syndrome reveals differences in clinical presentation between female and male patients[J]. Biol Sex Differ, 2017, 8 (1): 25.
doi: 10.1186/s13293-017-0146-6
12 Jara LJ , Navarro C , Brito-Zerón MDP , et al. Thyroid disease in Sjögren's syndrome[J]. Clin Rheumatol, 2007, 26 (10): 1601- 1606.
doi: 10.1007/s10067-007-0638-6
13 Williams DL , Pierce V , Mellor P , et al. Reduced tear production in three canine endocrinopathies[J]. J Small Anim Pract, 2007, 48 (5): 252- 256.
doi: 10.1111/j.1748-5827.2007.00349.x
14 Dias AC , MóDulo CM , Jorge ALG , et al. Influence of thyroid hormone on thyroid hormone receptor β-1 expression and lacrimal gland and ocular surface morphology[J]. Invest Ophth Vis Sci, 2007, 48 (7): 3038- 3042.
doi: 10.1167/iovs.06-1309
15 Kang YS , Lee HS , Li Y , et al. Manifestation of meibomian gland dysfunction in patients with Sjögren's syndrome, non-Sjögren's dry eye, and non-dry eye controls[J]. Int Ophthalmol, 2018, 38 (3): 1161- 1167.
doi: 10.1007/s10792-017-0577-4
16 Wang LX , Deng YP . Androgen and meibomian gland dysfunction: From basic molecular biology to clinical applications[J]. Int J Ophthalmol, 2021, 14 (6): 915- 922.
doi: 10.18240/ijo.2021.06.18
17 Satitpitakul V , Rattanaphong T , Pruksakorn V . Meibomian glands dropout in patients with inactive thyroid related orbitopathy[J]. PLoS One, 2021, 16 (4): e0250617.
doi: 10.1371/journal.pone.0250617
18 Altay M , Şahin T , Yildiz Z , et al. Changes in conjunctiva morphology using impression cytology in patients with Hashimoto's thyroiditis without thyroid-associated ophthalmopathy[J]. Turk Patoloji Derg, 2019, 35 (3): 213- 220.
19 Wang Q , Shangguan J , Zhang Y , et al. The prevalence of thyroid autoantibodies in autoimmune connective tissue diseases: A systematic review and meta-analysis[J]. Expert Rev Clin Immunol, 2020, 16 (9): 923- 930.
doi: 10.1080/1744666X.2020.1811089
20 解如山. 桥本甲状腺炎患者发生干眼症的相关联性分析[J]. 现代医药卫生, 2015, 31 (22): 3436- 3438.
21 Altin Ekin M , Karadeniz Ugurlu S , Egrilmez ED , et al. Ocular surface changes in Hashimoto's thyroiditis without thyroid ophthalmopathy[J]. Eye Contact Lens, 2021, 47 (1): 32- 37.
22 Xu J, Chen P, Yu C, et al. In vivo confocal microscopic evaluation of corneal dendritic cell density and subbasal nerve parameters in dry eye patients: A systematic review and meta-analysis[J/OL]. Front Med, 2021, 8: 578233[2021-07-01]. https://www.frontiersin.org/articles/10.3389/fmed.2021.578233/full.
23 Li F, Zhang Q, Ying X, et al. Corneal nerve structure in patients with primary Sjögren's syndrome in China[J/OL]. BMC Ophthalmol, 2021, 21(1): 211[2021-07-01]. https://bmcophthalmol.biomedcentral.com/articles/10.1186/s12886-021-01967-7.
24 Gabbriellini G , Baldini C , Varanini V , et al. In vivo confocal scanning laser microscopy in patients with primary Sjögren's syndrome: A monocentric experience[J]. Mod Rheumatol, 2015, 25 (4): 585- 589.
25 Levine H, Hwang J, Dermer H, et al. Relationships between activated dendritic cells and dry eye symptoms and signs[J/OL]. Ocul Surf, 2021, 21: 186-192[2021-07-01]. https://www.sciencedirect.com/science/article/pii/S1542012421000513?via%3Dihub.
26 Cardigos J , Barcelos F , Carvalho H , et al. Tear meniscus and corneal sub-basal nerve plexus assessment in primary Sjögren syndrome and sicca syndrome patients[J]. Cornea, 2019, 38 (2): 221- 228.
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[4] . [J]. Journal of Peking University(Health Sciences), 2002, 34(2): 112 -116 .
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