Journal of Peking University (Health Sciences) ›› 2022, Vol. 54 ›› Issue (6): 1106-1111. doi: 10.19723/j.issn.1671-167X.2022.06.008

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Clinical and immunological characteristics of systemic lupus erythematosus with retinopathy

Min LI1,Lin-qing HOU1,2,Yue-bo JIN1,Jing HE1,*()   

  1. 1. Department of Rheumatology and Immunology, Peking University People's Hospital, Bejing 100044, China
    2. Department of Rheumatology and Immunology, The Third People's Hospital of Linfen, Linfen 041000, Shanxi, China
  • Received:2022-08-14 Online:2022-12-18 Published:2022-12-19
  • Contact: Jing HE E-mail:hejing1105@126.com

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Abstract:

Objective: To investigate the clinical and immunological characteristics of systemic lupus erythematosus (SLE) with retinopathy. Methods: Fifty SLE patients with retinopathy without hypertension and diabetes (retinopathy group) who were hospitalized in the Peking University People's Hospital from January 2009 to July 2022 were screened. Fifty SLE patients without blurred vision during the course of the SLE and without retinopathy in the fundus examinations (non-retinopathy group) matched for sex and age were selected. Their clinical manifestations, laboratory tests and lymphocyte subsets were statistically analyzed. Results: The most common fundus ocular change of the SLE patients with retinopathy was cotton-wool spots (33/50, 66.0%), followed by intraretinal hemorrhage (31/50, 62.0%). Retinopathy could occur at any stage of SLE duration, with a median of 1 year (20 days to 30 years). The proportion of lupus nephritis (72.0% vs. 46.0%, P=0.008) and serositis (58.0% vs. 28.0%, P=0.002) in the retinopathy group were significantly higher than those in the non-retinopathy group. The proportion of neuropsychiatric systemic lupus erythematosus (NPSLE) in the retinopathy group was higher, but there was no significant difference between the two groups. Compared with the non-retinopathy group, the proportion of positive anti-cardiolipin antibody (30.0% vs. 12.0%, P=0.027), the SLEDAI score (median 22.0 vs. 10.5, P < 0.001), erythrocyte sedimentation rate (P < 0.001), C-reactive protein (P=0.019) and twenty-four hours urine total protein level (P=0.026) in the retinopathy group were significantly higher, and the hemoglobin level was significantly lower [(91.64±25.18) g/L vs. (113.96±18.57) g/L, P < 0.001]. The proportion of CD19+ B cells in peripheral blood of the patients with SLE retinopathy was significantly increased (P=0.010), the proportion of CD4+ T cells was significantly decreased (P=0.025) and the proportion of natural killer (NK) cells was lower (P=0.051) when compared with the non-retinopathy group. Conclusion: Retinopathy in SLE suggests a higher activity of SLE disease with more frequent hematologic and retinal involvement. It is recommended to perform fundus examination as soon as a patient is diagnosed with SLE. SLE patients with retinopathy may have stronger abnormal proliferation of B cells, and aggressive treatment should be applied to prevent other important organs involvement.

Key words: Systemic lupus erythematosus, Retinopathy, Clinical characteristics, Lymphocyte subsets

CLC Number: 

  • R593.24

Figure 1

Lupus retinopathy shown by fundus examinations A, cotton-wool spots; B, hemorrhages; C, cutton-wool spots and hemorrhages; D, vaso-occlusion."

Table 1

Clinical characteristics between the two groups"

Variable Retinopathy group (n=50) Non-retinopathy group (n=50) χ2/U P
SLEDAI, M (P25, P75) 22.00 (16.75, 29.00) 10.50 (6.0, 15.25) 223.5 < 0.001#
Fever, n (%) 13 (26.0) 12 (24.0) 0.053 0.817
Rash, n (%) 16 (32.0) 17 (34.0) 0.045 0.832
Hair loss, n (%) 8 (16.0) 6 (12.0) 0.332 0.564
Mucosal ulcer, n (%) 7 (14.0) 6 (12.0) 0.088 0.766
Arthritis, n (%) 9 (18.0) 10 (20.0) 0.065 0.799
Vasculitis, n (%) 4 (8.0) 5 (10.0) 0.000 1.000a
Myositis, n (%) 4 (8.0) 2 (4.0) 0.177 0.678a
NPSLE, n (%) 10 (20.0) 4 (8.0) 2.076 0.148a
Thrombocytopenia, n (%) 21 (42.0) 12 (24.0) 3.664 0.056
Leukopenia, n (%) 12 (24.0) 11 (22.0) 0.056 0.812
Cylindruria, n (%) 9 (18.0) 2 (4.0) 3.677 0.051a
Hematuria, n (%) 25 (50.0) 12 (24.0) 7.250 0.007*
Proteinuria, n (%) 30 (60.0) 20 (40.0) 4.000 0.046*
Pyuria, n (%) 23 (46.0) 7 (14.0) 12.190 < 0.001#
Lupus nephritis, n (%) 36 (72.0) 23 (46.0) 6.986 0.008*
Serositis, n (%) 29 (58.0) 14 (28.0) 9.180 0.002*

Table 2

Laboratory differences between the two groups"

Variable Retinopathy group (n=50) Non-retinopathy group (n=50) t/U P
Hb/(g/L), ${\bar x}$±s 91.64±25.18 113.96±18.57 4.838 < 0.001#
ESR/(mm/h), M (P25, P75) 42.00 (24.00, 64.50) 18.50 (7.00, 34.25) 583.5 < 0.001#
CRP/(mg/L), M (P25, P75) 2.91 (1.61, 6.76) 1.41 (0.56, 6.89) 654.0 0.019*
Alb/(g/L), ${\bar x}$±s 30.78±6.70 33.05±7.61 1.517 0.133
24 h-UTP/(g/d), M (P25, P75) 0.64 (0.22, 1.87) 0.19 (0.10, 1.44) 700.0 0.026*
ANA (+), n (%) 46 (92.0) 45 (90.0) 0.000 1.000a
Anti-dsDNA (+), n (%) 31 (62.0) 30 (60.0) 0.042 0.838
Anti-dsDNA/(IU/mL), M (P25, P75) 113.30 (29.80, 200.00) 49.60 (19.68, 200.00) 735.0 0.146
Anti-Sm antibody (+), n (%) 10 (20.0) 9 (18.0) 0.065 0.799
Anti-RNP antibody (+), n (%) 19 (38.0) 20 (40.0) 0.042 0.838
Anti-SSA antibody (+), n (%) 21 (42.0) 27 (54.0) 1.442 0.230
Anti-SSB antibody (+), n (%) 6 (12.0) 5 (10.0) 0.102 0.749
AnuA (+), n (%) 29(58.0) 24 (48.0) 1.004 0.316
AnuA/(RU/mL), M (P25, P75) 44.68 (8.23, 151.43) 22.63 (9.40, 186.42) 881.0 0.736
ACLA (+), n (%) 15 (30.0) 6 (12.0) 4.882 0.027*
ACLA/(U/mL), M (P25, P75) 4.60 (2.00, 11.40) 3.50 (2.15, 7.28) 878.5 0.364
Anti-β2 GP 1 (+), n (%) 15 (30.0) 10 (20.0) 1.477 0.224
Anti-β2 GP 1/(RU/mL), M (P25, P75) 6.72 (2.08, 37.14) 7.47 (2.83, 14.61) 931.5 0.773
LAC (+), n (%) 9 (18.0) 3 (6.0) 2.367 0.121a
LAC/s, M (P25, P75) 1.02 (0.95, 1.37) 0.99 (0.93, 1.13) 693.0 0.251
Coombs test (+), n (%) 29 (58.0) 20 (40.0) 7.241 0.072
IgA (g/L), ${\bar x}$±s 2.42±1.28 2.88±1.28 1.671 0.098
IgG/(g/L), M (P25, P75) 13.50 (10.25, 20.30) 13.90 (8.80, 19.00) 921.5 0.463
IgM/(g/L), M (P25, P75) 1.09 (0.56, 1.66) 0.90 (0.47, 1.36) 798.5 0.213
C3/(g/L), M (P25, P75) 0.41 (0.253, 0.627) 0.59 (0.385, 0.712) 704.5 0.006*
C4/(g/L), M (P25, P75) 0.05 (0.025, 0.130) 0.12 (0.046, 0.157) 755.5 0.018*

Table 3

Laboratory differences in SLE patients with retinopathy and without retinopathy"

Variable Retinopathy group Non-retinopathy group t/U P
CD3+ T cells/%, ${\bar x}$±s 62.86±13.95 68.95±12.88 1.241 0.228
CD4+ T cells/%, ${\bar x}$±s 26.28±6.48 33.46±11.03 2.357 0.025*
CD8+ T cells/%, ${\bar x}$±s 36.47±11.47 35.49±10.84 -0.244 0.809
CD19+ B cells/%, ${\bar x}$±s 28.50±15.37 16.49±9.89 -2.738 0.010*
NK cells (%), M (P25, P75) 3.65 (1.53, 7.13) 5.10 (4.25, 7.25) 74.000 0.051

Figure 2

The levels of CD4+T cells, CD8+T cells, CD19+B cells and NK cells in the peripheral blood of two groups A, the proportion of CD4+ T cells in the retinopathy group was significantly decreased (P=0.025); B, there was no significant difference in the proportion of CD8+T cells between the two groups; C, the proportion of CD19+ B cells was significantly increased in the retinopathy group (P=0.010); D, the proportion of NK cells was decreased in the retinopathy group, but there was no significant difference between the two groups (P=0.051). NK, natural killer cell; RG, retinopathy group; NRG, non-retinopathy group; ns, not significant. *P < 0.05."

1 Au A , O'Day J . Review of severe vaso-occlusive retinopathy in systemic lupus erythematosus and the antiphospholipid syndrome: Associations, visual outcomes, complications and treatment[J]. Clin Exp Ophthalmol, 2004, 32 (1): 87- 100.
doi: 10.1046/j.1442-9071.2004.00766.x
2 Moulton VR , Suarez-Fueyo A , Meidan E , et al. Pathogenesis of human systemic lupus erythematosus: A cellular perspective[J]. Trends Mol Med, 2017, 23 (7): 615- 635.
doi: 10.1016/j.molmed.2017.05.006
3 Dammacco R , Procaccio P , Racanelli V , et al. Ocular involvement in systemic lupus erythematosus: The experience of two tertiary referral centers[J]. Ocul Immunol Inflamm, 2018, 26 (8): 1154- 1165.
doi: 10.1080/09273948.2018.1501495
4 Yen YC , Weng SF , Chen HA , et al. Risk of retinal vein occlusion in patients with systemic lupus erythematosus: A population-based cohort study[J]. Br J Ophthalmol, 2013, 97 (9): 1192- 1196.
doi: 10.1136/bjophthalmol-2013-303265
5 Lanham JG , Barrie T , Kohner EM , et al. SLE retinopathy: Evaluation by fluorescein angiography[J]. Ann Rheum Dis, 1982, 41 (5): 473- 478.
doi: 10.1136/ard.41.5.473
6 Hochberg MC . Updating the American college of rheumatology revised criteria for the classification of systemic lupus erythematosus[J]. Arthritis Rheum, 1997, 40 (9): 1725.
7 Gladman DD , Ibanez D , Urowitz MB . Systemic lupus erythematosus disease activity index 2000[J]. J Rheumatol, 2002, 29 (2): 288- 291.
8 Md Noh UK , Zahidin AZA , Yong TK . Retinal vasculitis in systemic lupus erythematosus: An indication of active disease[J]. Clinics and Practice, 2012, 2 (2): 54.
doi: 10.4081/cp.2012.e54
9 Stafford-Brady FJ , Urowitz MB , Gladman DD , et al. Lupus retinopathy. Patterns, associations, and prognosis[J]. Arthritis Rheum, 1988, 31 (9): 1105- 1110.
doi: 10.1002/art.1780310904
10 Giorgi D , Pace F , Giorgi A , et al. Retinopathy in systemic lupus erythematosus: Pathogenesis and approach to therapy[J]. Hum Immunol, 1999, 60 (8): 688- 696.
doi: 10.1016/S0198-8859(99)00035-X
11 D'Cruz D . Vasculitis in systemic lupus erythematosus[J]. Lupus, 1998, 7 (4): 270- 274.
doi: 10.1191/096120398678920082
12 Kharel R , Shah DN , Singh D . Role of lupus retinopathy in systemic lupus erythematosus[J]. Ophthalmic Inflamm Infect, 2016, 6 (1): 1- 4.
doi: 10.1186/s12348-015-0068-6
13 Seth G , Chengappa KG , Misra DP , et al. Lupus retinopathy: A marker of active systemic lupus erythematosus[J]. Rheum Int, 2018, 38 (8): 1495- 1501.
doi: 10.1007/s00296-018-4083-4
14 曹绪胜, 纪海霞, 张永鹏, 等. 全身使用糖皮质激素继发中心性浆液性脉络膜视网膜病变的临床特征[J]. 眼科, 2020, 29 (3): 193- 197.
doi: 10.3969/j.issn.1006-8422.2020.03.001
15 Million M , Raoult D . The pathogenesis of the antiphospholipid syndrome[J]. N Engl J Med, 2013, 368 (24): 2335.
doi: 10.1056/NEJMc1300484
16 Jeon S , Lee WK . Aggravated capillary non-perfusion after intravitreal bevacizumab for macular edema secondary to systemic lupus erythematosus and anti-phospholipid syndrome[J]. Lupus, 2012, 21 (3): 335- 337.
doi: 10.1177/0961203311422095
17 Zhu W , Wu Y , Xu M , et al. Correction: Antiphospholipid antibody and risk of retinal vein occlusion: A systematic review and meta-analysis[J]. PLoS One, 2016, 11 (6): e157536.
18 Lipsky PE . Systemic lupus erythematosus: An autoimmune disease of B cell hyperactivity[J]. Nat Immunol, 2001, 2 (9): 764- 766.
doi: 10.1038/ni0901-764
19 Wei C , Anolik J , Cappione A , et al. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus[J]. J Immunol, 2007, 178 (10): 6624- 6633.
doi: 10.4049/jimmunol.178.10.6624
20 Hickman RA , Denniston AK , Yee CS , et al. Bilateral retinal vasculitis in a patient with systemic lupus erythematosus and its remission with rituximab therapy[J]. Lupus, 2010, 19 (3): 327- 329.
doi: 10.1177/0961203309347332
21 Damato E , Chilov M , Lee R , et al. Plasma exchange and rituximab in the management of acute occlusive retinal vasculopathy secondary to systemic lupus erythematosus[J]. Ocul Immunol Inflamm, 2011, 19 (5): 379- 381.
doi: 10.3109/09273948.2011.603069
22 Tselios K , Lam WC , Urowitz MB , et al. Rituximab for sight-threatening lupus-related retinal vasculitis[J]. J Clin Rheumatol, 2018, 24 (2): 93- 94.
doi: 10.1097/RHU.0000000000000600
23 Liu M , Liu J , Zhang X , et al. Activation status of CD56(dim) natural killer cells is associated with disease activity of patients with systemic lupus erythematosus[J]. Clin Rheumatol, 2021, 40 (3): 1103- 1112.
doi: 10.1007/s10067-020-05306-x
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