Systemic lupus erythematosusassociated optic neuritis: clinical experience and literature review
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1 Systemic lupus erythematosusassociated optic neuritis: clinical experience and literature review Yen-Ching Lin, 1,2,3 An-Guor Wang 2,3 and May-Yung Yen 2,3 1 Department of Ophthalmology, Suao Veterans Hospital, I-Lan, Taiwan 2 Department of Ophthalmology, Taipei Veterans General Hospital, Taipei, Taiwan 3 School of Medicine, National Yang Ming University, Taipei, Taiwan ABSTRACT. Purpose: This study aimed to evaluate the visual outcome of optic neuritis in patients with systemic lupus erythematosus (SLE). Methods: A retrospective, case-observational study was conducted by reviewing eight patients with SLE-associated optic neuritis from January 1986 to October The demographic data, clinical manifestations, laboratory data, medical management and disease courses of these eight patients were retrospectively analysed. Main outcome measurements included final visual acuity (VA) and relapse of optic neuritis. Statistical analyses were made using the chi-square test and a linear regression model. The English-language literature on SLE-associated optic neuritis was reviewed. Results: Initial visual loss was severe in SLE-associated optic neuritis. Seven patients (87%) had VA < at onset. All patients received steroid pulse therapy followed by oral steroid tapering. Final visual outcome was highly variable, ranging from the complete recovery of VA in four patients, to partial recovery in one and poor recovery in three. Better visual recovery occurred in patients who received earlier treatment (within 10 days). However, longer duration of steroid administration was found to have no significant benefit on visual outcome. Conclusions: Systemic lupus erythematosus-associated optic neuritis is not common. However, it is important that ophthalmologists differentiate SLEassociated optic neuritis from idiopathic optic neuritis because of the severe visual impairment and steroid dependence associated with the former. Early diagnosis and prompt treatment are important for restoring visual function in these patients. Key words: optic neuritis optic neuropathy SLE systemic lupus erythematosus Acta Ophthalmol. 2009: 87: ª 2008 The Authors Journal compilation ª 2008 Acta Ophthalmol doi: /j x Introduction Optic neuritis is an acute disease of the optic nerve with focal inflammation associated with demyelination, infectious disease, or autoimmunity (Smith 2005). Most cases of optic neuritis have an idiopathic aetiology and patients may recover spontaneously within months, even without steroid treatment (Smith 2005). However, patients with systemic lupus erythematosus (SLE) may experience an attack with the clinical manifestations of optic neuritis which is followed by an atypical course of disease progression and poor prognosis (Dutton et al. 1982). Optic neuritis is uncommon in SLE but may be the presenting feature of the disease. Ophthalmological and central nervous system (CNS) manifestations occur in 20 40% of patients with SLE (Feinglass et al. 1976; Smith 2005). Involvement of the optic nerve or chiasm is rare and occurs in only 1% of patients with SLE, typically after the diagnosis has been established and multiple other manifestations are present (Feinglass et al. 1976; Jabs et al. 1986; Smith 2005). Megadose steroid therapy followed by continued oral administrations of steroid or cytotoxic drugs are thought to be necessary to restore vision in these patients (Dutton et al. 1982; Kupersmith et al. 1988). However, visual outcomes in cases of SLE-associated optic neuritis reported in the literature have been poor (Smith & Pinals 1982; Jabs et al. 1986). Herein, we report eight patients with SLE-associated optic neuritis and analyse their clinical manifestations and visual recovery. Materials and Methods The initial database was compiled from recorded diagnoses of optic 204
2 neuritis for the period January 1986 to October 2004 held on the computer system of Taipei Veterans General Hospital. A total of 196 patients with a clinical diagnosis of optic neuritis were found. Eight patients who met the American Rheumatism Association s (ARA) revised criteria (Tan et al. 1982) for the classification of SLE were enrolled in our present study. A retrospective review of chart records was made according to a standard protocol whereby demographic and laboratory data and information on ophthalmic examinations, treatment modalities and clinical courses were extracted. Visual acuity (VA) was examined using a Snellen chart. Laboratory examinations included white cell counts, erythrocyte sedimentation rate (ESR), immunoglobulin (IgG IgA IgM), antinuclear antibodies (ANA), complement 3 4 (C3 C4), and anti-double strand DNA antibodies (anti-dsdna Ab). In three patients, anti-cardiolipin antibodies were also evaluated. Global disease activity was assessed by the SLE Disease Activity Index (SLEDAI) at the time-point when optic neuritis was diagnosed (Bombardier et al. 1992). These eight patients received steroid pulse therapy according to the protocol of the Optic Neuritis Treatment Trial (ONTT), with i.v. methylprednisolone (1.0 g day for 3 days), followed by oral prednisolone on day 4 of treatment, at 1 mg kg day tapered according to disease activity remission (Beck et al. 1992). The period from the onset of visual loss to the institution of treatment was recorded as treatment timing. The period from the beginning of pulse therapy to the discontinuance of oral steroid treatment was recorded as treatment duration. Any recurrence of optic neuritis was also recorded in each patient. All the above-mentioned risk factors were analysed statistically to evaluate their associations with the final visual outcome. Complete visual recovery was defined as VA and identification of Ishihara colour plates. Poor visual recovery was defined as VA Statistical analyses of the results were made using a chi-square test and linear regression model. A two-tailed result with a p-value < 0.05 was considered statistically significant. All statistical calculations were performed with spss software (Version ; SPSS Inc., Chicago, IL, USA). Results Demographic data Of the 196 patients with a clinical diagnosis of optic neuritis, eight met the diagnostic criteria for SLE (eight women). The remaining 188 patients (101 women, 87 men) had no SLE manifestations. The mean age at the first attack of optic neuritis was 32.4 ± 13.0 years (range 14)48 years) in patients with SLE and 41.2 ± 17.0 years (range 7)80 years) in patients without SLE. The mean age at diagnosis of SLE was 28.0 ± 9.7 years (range 14)38 years). Optic neuritis was presented as the initial manifestation of SLE in three patients (37.5%). The mean duration of follow-up was 7.8 ± 5.4 years (range 11 months to 15.2 years). Disease manifestations and past medications for SLE Three of the eight patients (Cases 1, 3 and 8) had no history of SLE or other autoimmune disease and presented acute vision loss as their initial manifestation of disease. The other five patients had been diagnosed with SLE under the ARA s revised criteria (Tan et al. 1982) before the optic neuritis attack (range 2)14 years). All these five patients were in a stable condition without evidence of active flare-up of SLE and were using maintenanceonly doses of oral steroids (range 5)15 mg day) when optic neuritis occurred. One patient (Case 7) also received azathioprine (Imuran) 100 mg day. Ophthalmic examination Pertinent details are summarized in Table 1. Initial VA was < in seven patients (87.5%). Final VA was highly variable, ranging from to counting fingers (CF). Pain on eye movement was present in five patients (62.5%). Fundus examination showed optic disc swelling in three patients (37.5%), pale discs in two patients (25%), and a normal disc appearance in three patients (37.5%). Fluorescein angiography was performed in five patients (Cases 4)8), only one of whom showed distinct fluorescent dye staining of the optic disc in the late phase. Laboratory data Leucopoenia (< 4000 cells mm 3 ) was present in three patients (37.5%). Hypocomplementaemia was found in four patients (50%). Hyperglobulinaemia was present in three patients (37.5%). Antinuclear antibodies (> 1 : 80 titre) were present in seven patients (87.5%). Antibodies to dsdna were detected in six patients (75%). Table 2 compares these laboratory data with findings in Hochberg et al. (1985). The autoantibodies to the SSA Ro and SSB/La ribonucleoprotein complex, which are specific in primary Sjogren s disease and SLE, were checked in two patients (Cases 1 and 8) during optic neuritis attack and were found to be negative. Anti- Sm antibodies were checked in only one patient (Case 1) during optic neuritis attack, again for a negative result. Anti-RNP (anti-riboneucleic protein) antibodies were checked in one patient (Case 1) and found to be positive. Lupus anticoagulant was checked in two patients and found to be positive in one (Case 4). Antibodies (IgG) to cardiolipin were determined in three patients and found to be positive in two (Cases 3 and 6). However, the clinical findings in these two patients did not meet the diagnostic criteria for anti-phospholipid syndrome. No history of venous thrombosis or recurrent fetal loss was noted in either of these patients. Neuroimaging studies Magnetic resonance imaging was performed in seven patients, five of whom demonstrated gadolinium enhancement over the orbital portion or perichiasmatic region of the optic nerve, which was well correlated with their lesion eye in laterality. Two showed bilateral involvement (Cases 7 and 8). Segmental enhancement of the optic nerve was noted in two patients (Cases 4 and 8). A 15-mm enhancement of the optic nerve was found in Case 4 (Fig. 1A). Case 8 demonstrated a 12-mm enhancement in the right optic nerve and a 5-mm enhancement in the left (Fig. 1B). 205
3 Table 1. Summary of demographic data, and clinical and laboratory findings for the eight systemic lupus erythematosus (SLE) patients with optic neuritis. Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Gender F F F F F F F F Age (years) at SLE diagnosis Age (years) at first ON attack Time (years): ON ) 1 after SLE Initial VA OD CF NLP HM OS CF CF LP Final VA OD OS CF Lesion eye OD OU OD OS OD OS OU OU Disc swelling (+) (+) ()) ()) (+) ()) ()) ()) Tx timing (days)* Tx duration (days) Follow-up (years) No. of relapses MRI findings ND Neg. Neg. Enhancement, optic nerve OS Enhancement, optic nerve OU Swelling, optic nerve OD Enhancement, prechiasmatic optic nerve lesion OS Enhancement, optic nerve OU * Time to start of steroid treatment (Tx) after the onset of vision loss in first attack of ON (days). Total duration of steroid administration for the first attack of ON (days). ON = optic neuritis; OD = right eye; OS = left eye; OU = both eyes; VA = visual acuity; CF = counting fingers; HM = hand movements LP = light perception; NLP = no light perception; ND = not done; Neg. = negative. Table 2. Laboratory tests. Present study (n =8) Hochberg et al. (1985) (n = 150) administration did not affect final vision (chi-square test, p > 0.5) (Table 3). Leucopoenia 3 (37.5) 62 (41) Antinuclear antibodies 7 (87.5) 141 (94) Hypocomplementaemia 4 (50) 89 (59) Hyperglobulinaemia 3 (37.5) 45 (30) Anti-dsDNA antibodies 6 (75) 134 (89) Values given in parentheses are percentages. Final visual outcome Three patients had bilateral involvement. Case 2 had a sequential involvement of bilateral optic nerves, with the right eye being affected first and the left eye becoming involved 3 years later. Case 7 had a concurrent involvement of both optic nerves during the same attack. In Case 8, the right eye became involved first, at the age of 38 years, and the left eye was affected 2 years later; both eyes were involved in a third attack. Final VA ranged from to CF. Four patients (50%) achieved a visual recovery to One patient achieved recovery from no light perception to The remaining three patients (37.5%) had poor visual recovery and eventually developed optic atrophy (Table 1). All patients received steroid pulse therapy. However, the timing of this treatment differed in each patient. The average start of treatment was 12.1 ± 6.1 days (range 5)21 days) after the onset of visual loss. The duration of steroid treatment varied depending on the response in each patient (Table 1). The average duration of treatment was 32.6 ± 21.7 days (range 13)70 days). We found that patients who received early treatment (within 10 days) achieved significantly better visual recovery than those in whom treatment was delayed (chi-square test, p < 0.025). However, the duration of steroid Relapse of optic neuritis Relapse of optic neuritis was noted in three patients (37.5%). There was a tendency for longer duration of steroid treatment to decrease the risk of optic neuritis relapse (linear regression, r 2 = ). Case Reports The clinical courses of three patients with recurrent attacks of optic neuritis are described as followed. Case 2 This patient was diagnosed with SLE at the age of 36 years. She suffered from a sudden onset of visual loss in the left eye at 42 years of age. Best corrected visual acuity (BCVA) was in the right eye and CF in the left eye. The patient was able to identify Ishihara colour plates with the right eye and none with the left. Two weeks after visual loss, pulse therapy with methylprednisolone was 206
4 (A) steroid treatment was administered for each attack of optic neuritis. Because of the repeated relapses of optic neuritis, the subject was maintained on oral steroid treatment (5 mg day) for 3 years after the last attack. Her final recorded vision was in the right eye, but the patient was lost to follow-up thereafter. (B) Fig. 1. (A) Magnetic resonance imaging (MRI) shows a 15-mm segmental enhancement of the optic nerve OS in Case 4. (B) Horizontal MRI shows segmental enhancements of the optic nerve of 12 mm OD and 5 mm OS in the second recurrence of optic neuritis in Case 8. Table 3. Visual recovery associated with the time of starting steroid treatment and the duration of steroid treatment. Vision recovery (n) administered for 3 days, followed by oral steroid treatment for 14 days. Partial recovery occurred in the left eye (BCVA ). Six years later, the subject experienced rapid visual loss to CF in the right eye. Pulse therapy was given within 3 days of this occurrence and was followed by oral steroid treatment, with gradual tapering for 24 days. The subject achieved complete recovery of vision in the right eye after treatment (BCVA 20 20). > to <20 25 (n) 20 25(n) p-value* Treatment start 10 days < > 10 days Treatment duration < 28 days > days * Chi-square test. Case 4 Case 4 was diagnosed with SLE at 38 years of age. Her first episode of optic neuritis occurred in the left eye when she was 40 years old. Best corrected VA was in the right eye and CF in the left. The subject s vision recovered completely after pulse therapy. However, she had four recurrences of optic neuritis in the same eye over a 7-year period. Pulse therapy followed by slow tapering of oral Case 8 Case 8 suffered from acute visual loss in her right eye at the age of 28 years. She had no past history of SLE. Vision was limited to hand movements (HM) in the right eye before treatment. A systemic survey including clinical and laboratory investigations for autoimmune disease was performed, but no positive results were found. Pulse therapy with oral steroid treatment was administered for 3 weeks. Vision recovered to The patient underwent a second attack of optic neuritis in the left eye 2 months later, but achieved a complete recovery of vision in this eye after steroid treatment. Unfortunately, she had a third attack of bilateral optic neuritis 3 months later. Her response to steroid treatment was poor and bilateral optic atrophy eventually developed (BCVA was OD and OS). Systemic evaluation was repeated during the third attack, with negative results. The diagnosis of SLE was finally made 1 year later, based on the presence of antinuclear antibodies, anti-dsdna antibodies, leucopoenia, proteinuria and arthritis. Discussion Optic neuropathy is relatively uncommon in the course of SLE, with a prevalence of approximately 1% (Feinglass et al. 1976). Optic neuropathy associated with SLE can manifest as acute retrobulbar optic neuritis, papillitis, anterior ischaemic optic neuropathy, posterior ischaemic optic neuropathy, or slow, progressive visual loss (Singerman & Jampol 1991). The pathogenic mechanism of SLE-associated optic neuropathy has been considered as different from those of idiopathic optic neuritis. It may manifest as a thrombotic, vasoocclusive event with focal axonal necrosis, or as a general immunologi- 207
5 cal inflammation, such as vasculitis. However, even with current sophisticated diagnostic testing, it is sometimes hard to distinguish clinically between ischaemic optic neuropathy and optic neuritis (Jabs et al. 1986; Rizzo & Lessell 1991; Giorgi & Balacco Gabrieli 1999). Irrespective of its underlying pathogenesis, we propose to ascribe a clinical diagnosis of SLEassociated optic neuritis to our patients. The mean age of the first attack of optic neuritis (32.4 years) in our patients with SLE was lower than the mean age at onset of idiopathic optic neuritis (41.2 years) and similar to the mean age reported by the Optic Neuritis Study Group (1991) (31.8 years). Female sex is a significant feature of optic neuritis associated with SLE. All the patients with SLE-associated optic neuritis in our study were female. Only 53.7% of our patients with idiopathic optic neuritis and 77.2% of the patients reported by the Optic Neuritis Study Group (1991) were female. Ophthalmologists should be alert to this when a young female patient presents with acute vision loss. Further evaluation of the relative profiles of SLE is important. Profound visual impairment is characteristic of SLE-associated optic neuritis. Poor VA at onset was reported in three of four patients by Smith & Pinals (1982) and in all of seven patients by Siatkowski et al. (2001). In our study, seven of eight patients (87.5%) had VA < at onset. Findings of poor VA at onset may be helpful in distinguishing SLE-associated optic neuritis from optic neuritis in multiple sclerosis (MS) (Singerman & Jampol 1991). In the ONTT, only 35.9% of patients had initial VA < (Optic Neuritis Study Group 1991). Optic neuritis associated with SLE results in more severe visual impairment than idiopathic optic neuritis does. This may reflect the different pathogenesis of optic neuritis in SLE, which is not a true infection or inflammation of the nerve tissue itself but is related to ischaemia, which may produce demyelination alone, axonal necrosis, or a combination of the two (Smith 2005). Histopathological evidence of a focal ischaemic lesion of the optic nerve caused by lupus vasculitis was reported by Hackett et al. (1974). In addition, demyelination and necrosis of optic nerve was noted in April & Vansonnenberg (1976). Poor visual recovery is characteristic of SLE-associated optic neuritis. In the ONTT, 87% of patients achieved VA after 5 years (Optic Neuritis Study Group 1997). In our study of SLE-associated optic neuritis, only four patients (50%) achieved a final VA Three of our patients (37.5%) developed optic atrophy with final VA Similar results of poor visual recovery have been reported in the literature (Table 4) (Hackett et al. 1974; Cinefro & Frenkel 1978; Smith & Pinals 1982; Jabs et al. 1986; Siatkowski et al. 2001). The most probable pathogenesis for the poor visual outcome may concern the irreversible nature of occlusive vasculitis involving the small arterioles of the optic nerve, which results in axonal loss and permanent nerve tissue damage (Hackett et al. 1974; Smith 2005). We assessed the autoimmunity status of our patients with reference to the cumulative laboratory data reported by Hochberg et al. (1985). We found no significant difference between results for our patients and results for all SLE patients in Hochberg et al. (1985) (Table 2). The most commonly used assessment of SLE disease activity, the Systemic Lupus Erythematosus Disease Activity Index (SLEDAI), was first described in Bombardier et al. (1992). It includes nine organ systems with different weighted index scores. We examined the relationships between disease activity and optic nerve involvement in our patients, with particular focus on haematological and serological findings (Table 5). The results showed that an attack of optic neuritis can occur even in periods of low disease activity in SLE. Occurrence of optic neuritis is not related to systemic disease activity in SLE. Ophthalmologists should be aware that optic neuritis may occur at any stage in SLE patients, even in the laboratory silence of a period of low disease activity. We found a segmental enhancement in the involved optic nerve in MRI, whereby the longer the optic nerve enhancement is, the more severe the initial visual loss will be. However, the final visual outcome seems to be unrelated to the length of enhancement in the two patients reported here. Although the clinical features of SLE-associated optic neuritis differ greatly from those of idiopathic optic neuritis, pulse therapy with megadose steroid treatment is still recommended for acute optic neuritis in SLE Table 4. Visual acuity (VA) in patients with systemic lupus erythematosus-associated optic neuritis reported in the literature. Authors Case number Initial VA <20 200, n (%) Final VA >20 25, n (%) Hackett et al. (1974) 3 2 (66.7) 0 (0) Smith & Pinals (1982) 4 3 (75) 1 (25) Jabs et al. (1986) 7 3 (42.9) 3 (42.9) Siatkowski et al. (2001) 6 6 (100) 1 (16.7) Present study (2005) 8 7 (87.5) 4 (50) Optic Neuritis Treatment Trial (1991) (35.9) 390 (87) Table 5. Haematological and serological features of systemic lupus erythematosus disease activity during optic neuritis. Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Leucopoenia ) ) ) + + ) ) + Thrombocytopoenia + ) ) + + ) + ) dsdna antibodies + ) ) + + flcomplement + ) ) ) ) SLEDAI score The Systemic Lupus Erythematosus Disease Activity Index (SLEDAI; Bombardier et al. 1992) was assessed at the time of optic neuritis attack. 208
6 (Hackett et al. 1974; Smith & Pinals 1982; Jabs et al. 1986; Arevalo et al. 2002). Before optic atrophy develops, SLE-associated optic neuritis may respond dramatically to steroid treatment (Siatkowski et al. 2001). However, recrudescence during steroid tapering was common, requiring re-treatment with i.v. methylprednisolone and either chronic oral steroids or immunosuppressive agents (Siatkowski et al. 2001). Intravenous cyclophosphamide administration was considered as an alternative and more efficient therapy for SLE-associated optic neuritis, with fewer side-effects than steroid treatment (Rosenbaum et al. 1997; Galindo-Rodriguez et al. 1999; Barile-Fabris et al. 2005). None of our patients received i.v. cyclophosphamide, any other immunosuppressive medication or anti-malaria agents for the treatment of SLE-associated optic neuritis. Rheumatologists were consulted routinely during the hospitalization of our patients. None of our patients were given i.v. cyclophosphamide or other immunosuppressive medications while they were in a stable condition without evidence of systemic flare-up. However, three of our patients were given i.v. cyclophosphamide, azathioprine or hydroxycholoquine by rheumatology specialists in our hospital for the treatment of severe systemic SLE flare-up. Barile- Fabris et al. (2005) noted significant improvement in visual function in patients with SLE-associated optic neuritis treated with i.v. cyclophosphamide. According to the beneficial results reported in previously published series (Rosenbaum et al. 1997; Galindo-Rodriguez et al. 1999; Barile- Fabris et al. 2005), cyclophosphamide appears to be more effective than methylprednisolone in patients with SLE-associated optic neuritis. We would consider alternative treatments, such as cyclophosphamide or azathioprine, in the treatment of SLE-associated optic neuritis patients in the future. In our study, the duration of steroid treatment varied depending on the clinical response in each patient: the average length of an optic neuritis attack was 32.6 days. However, the duration of steroid administration did not statistically affect the final visual outcome. Optic neuritis recurred in three patients (37.5%). A maintenance dose of oral steroid treatment was used for several months in two of these patients. We observed a tendency for longer duration of steroid treatment to correlate with fewer recurrences of optic neuritis. Four of our patients achieved good visual recovery after steroid pulse therapy. We found the timing of treatment to be important to the management of SLE-associated optic neuritis. Patients who received early treatment (within 10 days) made a significantly better visual recovery than those with delayed management. Meyer et al. (2001) found that acute neuron apoptosis occurred within hours of the onset of optic neuritis, with an inflammatory attack against myelin components in a rat model of experimental autoimmune encephalomyelitis (EAE). Hobom et al. (2004) found that neuronal cell death occurred before the onset of clinical symptoms in the demyelinating model. However, the nature of neuronal cell death in SLE-associated optic neuritis has not been well established. The fact that early treatment resulted in better final outcomes in our patients may indicate that neuron damage occurs considerably early in the course of SLE-associated optic neuritis. Although this study is limited by its small sample size, it is clear that early diagnosis of SLE-associated optic neuritis and early treatment with pulse therapy result in a better prognosis. Severe visual impairment and poor visual recovery may be caused by acute neuron apoptosis in the early stage of an SLE-associated optic neuritis attack. 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