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ORIGINAL ARTICLE
Ahead of print publication  

Changing etiology of sympathetic ophthalmia: A 10-year study from a tertiary referral center in Taiwan


1 Department of Ophthalmology, Kaohsiung Veterans General Hospital; Department of Optometry, Shu-Zen Junior College of Medicine and Management, Kaohsiung, Taiwan
2 Department of Ophthalmology, Kaohsiung Medical University Hospital; School of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
3 Department of Ophthalmology, Kaohsiung Veterans General Hospital, Kaohsiung; Department of Ophthalmology, School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan

Date of Submission25-Jul-2022
Date of Acceptance31-Oct-2022
Date of Web Publication11-Jan-2023

Correspondence Address:
Shih-Chou Chen,
No. 386, Dazhong 1st Rd., Zuoying, Kaohsiung 813
Taiwan
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/tjo.TJO-D-22-00094

  Abstract 


PURPOSE: In this study, we describe our experience of sympathetic ophthalmia (SO) at a tertiary referral center in Taiwan.
MATERIALS AND METHODS: We retrospectively analyzed records of patients diagnosed with SO from January 2011 to December 2020.
RESULTS: We collected data of 15 patients diagnosed with SO (eight males, seven females). Six patients developed SO after ocular penetrating trauma, and nine developed SO after ocular surgery, including seven with vitrectomy, one with penetrating keratoplasty, and one with cataract surgery. Penetrating ocular trauma was the primary cause of SO in the first 5 years (four of six cases), but the proportion was much lower in the last 5 years (two of nine cases). The interval between trigger events and SO ranged from 0.2 to 120 months. Nine patients received oral steroids alone, five patients received methylprednisolone pulse therapy followed by oral steroids, and immunosuppressants were added in four cases. Visual acuity of sympathetic eyes and exciting eyes improved after treatment. The initial visual acuity of sympathetic eyes in trauma related and ocular surgery related revealed no significant difference, but the final visual acuity of sympathetic eyes was better in ocular surgery-related cases than in the trauma-related cases (mean ± standard deviation, 1.01 ± 1.33 versus 0.49 ± 0.68 logarithm of the minimum angle of resolution, P = 0.021).
CONCLUSIONS: With the increased number of eye surgeries performed in recent years, eye surgery has emerged as the dominant etiology of SO in our 10-year study. Early detection and proper treatment help to maintain vision in most of the SO patients.

Keywords: Sympathetic ophthalmia, Taiwan, uveitis



How to cite this URL:
Chen SC, Sheu SJ, Wu TT. Changing etiology of sympathetic ophthalmia: A 10-year study from a tertiary referral center in Taiwan. Taiwan J Ophthalmol [Epub ahead of print] [cited 2023 Jan 28]. Available from: https://www.e-tjo.org/preprintarticle.asp?id=367589




  Introduction Top


Sympathetic ophthalmia (SO) is a rare, bilateral, diffuse granulomatous, nonnecrotizing panuveitis. It may develop after surgery or trauma of one eye, known as the exciting eye, and it is followed by a latent period of uveitis in the other eye, known as the sympathetic eye. SO presents with intraocular inflammation that may include exudative retinal detachment, anterior granulomatous inflammation with mutton-fat keratic precipitates, optic nerve inflammation, and macular edema in severe or chronic recurrent cases.[1],[2] Late diagnosis and treatment of SO may lead to irreversible loss of vision in both eyes. Blindness in one eye has less severe impact on life than bilateral eyes; blindness in both eyes has a huge impact on both the patient and their family and causes a heavy burden on society. To investigate the risk factors, clinical presentation, visual outcomes, and prognostic factors of patients with SO, we conducted a 10-year, retrospective chart review study of all the cases of SO in our hospital, a tertiary medical center in southern Taiwan.


  Materials and Methods Top


This study was a 10-year consecutive case series of patients diagnosed with SO between January 2011 and December 2020 at a tertiary referral center. The diagnosis of SO was established according to the classification criteria established by the Standardization of Uveitis Nomenclature (SUN) Working Group in 2021, and the diagnosis of SO includes bilateral uveitis with: (1) a history of unilateral ocular trauma or surgery and (2) an anterior chamber and vitreous inflammation or a panuveitis with choroidal involvement.[3] Patients with uveitis were surveyed. Cases who met the diagnostic criteria of SO were included, and cases who did not meet the diagnostic criteria or were identified as other causes of uveitis were excluded. This study was approved by the relevant institutional review board and ethics committee and adhered to the tenets of the Declaration of Helsinki (approval number: VGHKS19-CT7-06). The requirement of patient consent was waived due to the retrospective nature of the study. Ophthalmologic consultation was performed at the request of the physician during admission to the hospital, or the patient visited the clinic because of ocular symptoms. Data on demographic and clinical variables, including age, sex, ocular trauma history, ocular surgery history, duration of ocular symptoms, interval between triggering events and SO, duration of follow-up, and details of treatment, were collected. Ophthalmic examinations included assessment of initial and final visual acuity, slit-lamp biomicroscopy, intraocular pressure, indirect ophthalmoscopy or ultrasonography, optical coherence tomography (OCT), and fluorescein angiography (FAG) of exciting eyes and sympathetic eyes. Visual acuity values were recorded as Snellen or logarithm of the minimum angle of resolution (logMAR), and Snellen values were converted to logMAR for analyses. LogMAR values corresponding to count fingers, hand movements, perception of light (LP), and no LP (NLP) were substituted with 2.10, 2.40, 2.70, and 3.00 logMAR, respectively.[4] The scoring scale of anterior chamber inflammation was recorded as cell ranging from 0.5 + to 4 + according to the SUN Working Group.[3] Statistical analyses were performed using SPSS software version 20.0 (SPSS, Chicago, IL, USA). Descriptive statistics are expressed as the mean with standard deviation (SD). The means of normally distributed variables were compared with the t-test. The P value or 95th percentile confidence interval was calculated when appropriate, and comparisons were regarded as statistically significant at P < 0.05.


  Results Top


Fifteen patients diagnosed with SO, including eight (53.3%) male patients and seven (46.7%) female patients, were included. The average age of the affected patients was 58.40 ± 22.39 years (range: 6–86 years). Six patients developed SO after ocular penetrating trauma, and nine patients developed SO after ocular surgery. Among these nine patients, there were seven patients with vitrectomy, one patient with penetrating keratoplasty, and one patient with cataract surgery. No obvious complication or eventful phacoemulsification course was seen in the case with cataract surgery. Among the six patients with ocular penetrating trauma, there were four patients with eyeball rupture and two patients with corneal ulcer perforation. The interval between trigger events and presentation of SO was quite variable with an average of 26.53 ± 35.95 months (range: 0.2–120 months) [Table 1].
Table 1: Triggering event of patients with sympathetic ophthalmia

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In the indication of seven cases with vitrectomy, four were rhegmatogenous retinal detachment, one was tractional macular edema, one was macular pucker with intraocular lens dislocation, and one was vitreous hemorrhage. Four patients had sutured ports and three patients were sutureless. Regarding the sclerotomy gauge, four were 23-gauge and three were 20-gauge. No wound leakage was recorded in the vitrectomy cases [Table 2].
Table 2: Patients with triggering event of vitrectomy

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In clinical presentations of the sympathetic eye, anterior chamber inflammation and vitreous inflammation were seen in all patients. Keratic precipitates were seen in 12 patients (80%) and corneal edema was seen in two patients (13.3%). Fundus examinations revealed serous retinal detachment in six patients (40%), macular edema in three patients (20%), and Dalen-Fuchs nodule in one patient (6.7%). Serous retinal detachment was the most common finding and confirmed by OCT [Figure 1] and [Figure 2]. FAG was performed in some cases, revealing multiple hyperfluorescent leaking points with late-phase dye pooling and disc leakage helping to confirm the diagnosis [Figure 2]. Nine patients (60%) presented with panuveitis, two patients (13.3%) presented with anterior and intermediate uveitis, and four patients (26.7%) presented with anterior uveitis with vitreous inflammation. Systemic manifestations including tinnitus, headache, or alopecia [Figure 3] were observed in four patients (26.7%). The presentation of exciting eyes varied, which included anterior uveitis, panuveitis, serous retinal detachment, optic disc inflammation, phthisis bulbi, and prosthetic eye [Table 3] and [Figure 4].
Figure 1: (a) OCT showing serous retinal detachment in the sympathetic eye of patient 10. (b) Color fundus photo revealing vitreous opacity with serous retinal detachment. OCT = Optical coherence tomography

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Figure 2: Patient 12 was a case of SO that occurred after smooth cataract surgery. (a and b) OCT showing serous retinal detachment in both the OD (sympathetic eye) and OS (exciting eye). (c and d) FAG showing multiple leaking points confirming the diagnosis of SO. (e and f) Color fundus photo revealing serous retinal detachment in both eyes. Her panuveitis subsided after methylprednisolone pulse therapy, followed by oral steroids, and oral cyclosporine use. SO = Sympathetic ophthalmia, OCT = Optical coherence tomography, OD = Right eye, OS = Left eye, FAG = Fluorescein angiography

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Figure 3: Patient 1 was a case with eyeball rupture OD owing to family violence, and she refused treatment owing to personal factors. (a) Alopecia is seen. (b) Color fundus photo showing sunset-glow fundus. Alopecia and ocular inflammation resolved after oral steroid, but she disappeared again. Eight years later, she came back with subsequent vision loss in sympathetic eye. OD = Right eye

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Figure 4: Patient 4 was a case with eyeball rupture status post primary repair with bulbar atrophy OD. Five years after the ocular trauma, he had blurred vision in OS for 3 months. (a) OCT showing serous retinal detachment in the sympathetic eye. (b) Color fundus photo revealing vitreous opacity, serous retinal detachment, Dalen-Fuchs nodule, and retinal hemorrhages. Despite the panuveitis, vitreous opacity, and serous detachment subsided after intensive treatment, his vision was lost. OD = Right eye, OS = Left eye, OCT = Optical coherence tomography

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Table 3: Clinical presentations of the sympathetic eye in patients with sympathetic ophthalmia

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Initial visual acuity of the sympathetic eye ranged from hand motion to 6/6 or 2.4 to 0 logMAR (mean ± SD, 0.98 ± 0.82 logMAR). After treatment, the final visual acuity of the sympathetic eye ranged from NLP to 6/5 or 3 to − 0.08 logMAR (mean ± SD, 0.69 ± 0.98 logMAR). The improvement in visual acuity was statistically significant by pairwise comparison in the sympathetic eyes (P = 0.018). Visual improvement of the sympathetic eye was seen in 12 patients (80%) after treatment. Most of the sympathetic eyes (12/15, 80%) maintained a visual acuity of 6/60 or better, and good vision with 6/12 or better acuity was seen in nine patients (60%) at the last follow-up.

Initial visual acuity of the exciting eye ranged from no light perception to 6/8.6 or 3 to 0.16 logMAR (mean ± SD, 2.13 ± 0.90 logMAR). After treatment, the final visual acuity of the exciting eye ranged from NLP to 6/6 or 3 to 0 logMAR (mean ± SD, 1.88 ± 1.21 logMAR). Visual improvement in the exciting eye was seen in five patients (33.3%). Most of the exciting eyes (11/15, 73.3%) presented with poor visual acuity of <6/60 at the last follow-up [Table 4].
Table 4: Visual acuity and treatment of patients with sympathetic ophthalmia

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A comparison of the visual acuity of sympathetic eyes in trauma-related and ocular surgery-related cases revealed no significant difference in the initial visual acuity (mean ± SD, 1.06 ± 0.99 versus 0.92 ± 0.75 logMAR, P = 0.408). However, the final visual acuity after treatment was better in the ocular surgery-related cases than in the trauma-related cases (mean ± SD, 1.01 ± 1.33 versus 0.49 ± 0.68 logMAR, P = 0.021).

Regarding treatment, all patients received systemic treatment. Nine patients (60%) received oral steroids alone, five patients (33.3%) received intravenous methylprednisolone pulse therapy followed by oral steroids, and immunosuppressants were added in four patients (26.7%). Oral steroids were administered in all patients starting at a dose of 1 mg/kg body weight, and then tapered gradually for at least 3–6 months. None of the patients suffered from any severe side effects. All patients received a follow-up time of at least 3 months, with an average duration of 22.00 ± 26.36 months (range: 3–56 months) [Table 4].

Recurrent uveitis was only seen in two patients (patients 10 and 15) and inflammation subsided after increased doses of both steroids and immunosuppressants. All patients were stable with no recurrent uveitis for at least 3 months at the last follow-up.


  Discussion Top


The incidence of SO was reported to be 0.01% following intraocular surgery and 0.2%–0.5% following open-globe injuries.[5] In a recent meta-analysis study including 24 studies, the estimated overall incidence rate of SO after open-globe injury was 0.19%.[6] The prevalence of SO following penetrating ocular trauma is reported to be higher than that following ocular surgery in earlier literature. In the study by Gass in 1982, he reported the prevalence of SO at 0.01% following pars plana vitrectomy, and a prevalence of 0.06% after other types of penetrating ocular trauma.[7] However, ocular surgery – particularly vitreoretinal surgery – emerged as the main risk in recent years.[8] Postsurgical SO was analyzed in a study in 2018, which showed that vitreoretinal surgery was the most common inciting surgery, followed by cataract surgery.[9] The changing trend of etiology from ocular trauma to ocular surgery in SO cases was also found in our study, and vitreoretinal surgery was the most common inciting surgery. In a previous report about patterns and etiologies of uveitis at a tertiary referral center in Taiwan, SO accounted for only 5 of 450 (1.11%) of uveitis cases.[10] Although SO is a rare etiology of uveitis, it should still be considered an important differential diagnosis in uveitis patients with a history of ocular penetrating trauma or intraocular surgery.

In our 10-year follow-up of SO cases, trauma was the main cause of SO in the first 5 years (four of six cases, 66.7%, 2011–2015), but the proportion of trauma was lower in the latter 5 years (two of nine cases, 22.2%, 2016–2020). Interestingly, this trend was also seen in previous reports whereby ocular surgery – especially vitreoretinal surgery – had overtaken nonsurgical trauma as the major cause of SO.[8],[11],[12] With the progress of sutureless microincision vitrectomy surgery in recent years, the substantial increase in the amount of vitreoretinal surgery may account for the finding that ocular surgery has replaced penetrating ocular trauma as the main reason for SO in some studies, especially in developed countries, such as Singapore, Ireland, and the United Kingdom.[8],[11] In a recent case report from Japan, it was reported that there is still a risk of SO occurring in the eyes of patients who undergo transconjunctival vitrectomy, even if the sclerotomy site is as small as 27-G.[13] In developing countries, such as India and Mexico, penetrating ocular trauma remains the main cause of SO.[14],[15] In a commentary by Kilmartin et al., they mentioned that the risk of SO following vitrectomy was more than twice the risk of infectious endophthalmitis.[12],[16] Ophthalmologists will inform patients of the risk of infection before vitrectomy, but we should also consider allowing patients to understand the risk of SO before vitreoretinal surgery.

The time between ocular injury or surgery of the inciting eye to development of SO is quite varied, reportedly between 5 days and 66 years.[15],[17] In an earlier review in 1980, 80% of SO cases occurred within 3 months after injury to the exciting eye and 90% within 1 year.[18] In a study in 2000, 33% of cases occurred within 3 months, and only less than half of the cases occurred within 1 year.[19] In our study, 40% of cases (6/15) occurred within 3 months, and a higher ratio (53.3% of cases [8/15]) occurred within 1 year.

Symptoms and signs of SO included photophobia, redness, blurred vision, and other rarely seen systemic manifestations in our study. The ocular findings of SO included granulomatous anterior uveitis, posterior synechiae, fluctuation of intraocular pressure, vitritis, Dalen-Fuchs nodules, and exudative retinal detachment. In the sympathetic eyes of our cases, five of six (83.3%) patients with exudative retinal detachment presented with initial visual acuity of <6/12, and four of nine (44.4%) patients without exudative retinal detachment presented with initial visual acuity of <6/12. Exudative retinal detachment was associated with poorer vision, which is also seen in a previous study by Galor et al.[20] SO and Vogt–Koyanagi–Harada disease may present with similar systemic manifestations, including cerebrospinal fluid pleocytosis, sensory neural hearing disturbance, alopecia, poliosis, and vitiligo.[21] In our study, alopecia, headache, tinnitus, and neck stiffness were seen [Table 3] and [Figure 3].

The main therapy for SO is immunomodulatory therapy. With prompt and aggressive systemic immunomodulation, the visual prognosis of SO is good. In our study, most of the sympathetic eyes (12/15, 80%) maintained a visual acuity of 6/60 or better, and the visual acuity of sympathetic eyes improved from 0.98 ± 0.82 to 0.69 ± 0.98 logMAR at the last follow-up. The initial visual acuity of sympathetic eyes in trauma related and ocular surgery related revealed no significant difference, but the final visual acuity of sympathetic eyes was better in the ocular surgery-related cases than in the trauma-related cases (mean ± SD, 1.01 ± 1.33 versus 0.49 ± 0.68 logMAR, P = 0.021). This result was first mentioned in our study, and it reminds us that the overall visual prognosis of SO might be better with the trend of changing etiology from ocular penetrating injury to eye surgery. Although SO is a terrible disease that may cause blindness in both eyes, early diagnosis and treatment may allow most patients to obtain good final vision in sympathetic eyes.


  Conclusions Top


The key to management of SO is early diagnosis and prompt and adequate systemic therapy. With early diagnosis and proper treatment, patients often have good visual outcomes. Here, we shared our 10-year experience of SO in a tertiary referral center in Taiwan. Regarding the cause of SO, the proportion of eye surgery has increased in recent years, which might have contributed to the huge growth of sutureless microincision vitrectomy surgery in recent years. Although the final vision of sympathetic eyes was better in ocular surgery-related SO cases than trauma-related SO cases in our study, we suggest ophthalmologists should still pay attention to the occurrence of SO after ocular surgery, which may cause bilateral blindness.

Financial support and sponsorship

Nil.

Conflicts of interest

The authors declare that there are no conflicts of interests of this paper.



 
  References Top

1.
Duke-Elder S, Perkins ES. Sympathetic ophthalmitis. In: Duke-Elder S, editor. Diseases of the Uveal Tract. St. Louis: Mosby Press; 1966. p. 558-93.  Back to cited text no. 1
    
2.
Chu XK, Chan CC. Sympathetic ophthalmia: To the twenty-first century and beyond. J Ophthalmic Inflamm Infect 2013;3:49.  Back to cited text no. 2
    
3.
Standardization of Uveitis Nomenclature (SUN) Working Group. Classification criteria for sympathetic ophthalmia. Am J Ophthalmol 2021;228:212-9.  Back to cited text no. 3
    
4.
Day AC, Donachie PH, Sparrow JM, Johnston RL, Royal College of Ophthalmologists' National Ophthalmology Database. The royal college of ophthalmologists' national ophthalmology database study of cataract surgery: Report 1, visual outcomes and complications. Eye (Lond) 2015;29:552-60.  Back to cited text no. 4
    
5.
Marak GE Jr. Recent advances in sympathetic ophthalmia. Surv Ophthalmol 1979;24:141-56.  Back to cited text no. 5
    
6.
He B, Tanya SM, Wang C, Kezouh A, Torun N, Ing E. The incidence of sympathetic ophthalmia after trauma: A meta-analysis. Am J Ophthalmol 2022;234:117-25.  Back to cited text no. 6
    
7.
Gass JD. Sympathetic ophthalmia following vitrectomy. Am J Ophthalmol 1982;93:552-8.  Back to cited text no. 7
    
8.
Kilmartin DJ, Dick AD, Forrester JV. Prospective surveillance of sympathetic ophthalmia in the UK and Republic of Ireland. Br J Ophthalmol 2000;84:259-63.  Back to cited text no. 8
    
9.
Dutta Majumder P, Anthony E, George AE, Ganesh SK, Biswas J. Postsurgical sympathetic ophthalmia: Retrospective analysis of a rare entity. Int Ophthalmol 2018;38:2487-93.  Back to cited text no. 9
    
10.
Chen SC, Chuang CT, Chu MY, Sheu SJ. Patterns and etiologies of uveitis at a tertiary referral center in Taiwan. Ocul Immunol Inflamm 2017;25:S31-8.  Back to cited text no. 10
    
11.
Su DH, Chee SP. Sympathetic ophthalmia in Singapore: New trends in an old disease. Graefes Arch Clin Exp Ophthalmol 2006;244:243-7.  Back to cited text no. 11
    
12.
Kilmartin DJ, Dick AD, Forrester JV. Sympathetic ophthalmia risk following vitrectomy: Should we counsel patients? Br J Ophthalmol 2000;84:448-9.  Back to cited text no. 12
    
13.
Takai Y, Sakanishi Y, Okamoto M, Ebihara N. Sympathetic ophthalmia after 27-G pars plana vitrectomy. BMC Ophthalmol 2021;21:195.  Back to cited text no. 13
    
14.
Guzman-Salas PJ, Serna-Ojeda JC, Guinto-Arcos EB, Pedroza-Seres M. Characteristics of sympathetic ophthalmia in a single international center. Open Ophthalmol J 2016;10:154-9.  Back to cited text no. 14
    
15.
Chawla R, Kapoor M, Mehta A, Tripathy K, Vohra R, Venkatesh P. Sympathetic Ophthalmia: Experience from a tertiary care center in Northern India. J Ophthalmic Vis Res 2018;13:439-46.  Back to cited text no. 15
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16.
Kattan HM, Flynn HW Jr., Pflugfelder SC, Robertson C, Forster RK. Nosocomial endophthalmitis survey. Current incidence of infection after intraocular surgery. Ophthalmology 1991;98:227-38.  Back to cited text no. 16
    
17.
Zaharia MA, Lamarche J, Laurin M. Sympathetic uveitis 66 years after injury. Can J Ophthalmol 1984;19:240-3.  Back to cited text no. 17
    
18.
Lubin JR, Albert DM, Weinstein M. Sixty-five years of sympathetic ophthalmia: A clinicopathologic review of 105 cases (1913-1978). Ophthalmology 1980;87:109-21.  Back to cited text no. 18
    
19.
Bilyk JR. Enucleation, evisceration, and sympathetic ophthalmia. Curr Opin Ophthalmol 2000;11:372-86.  Back to cited text no. 19
    
20.
Galor A, Davis JL, Flynn HW Jr., Feuer WJ, Dubovy SR, Setlur V, et al. Sympathetic ophthalmia: Incidence of ocular complications and vision loss in the sympathizing eye. Am J Ophthalmol 2009;148:704-10.e2.  Back to cited text no. 20
    
21.
Chuang CT, Huang PS, Chen SC, Sheu SJ. Reversible alopecia in Vogt-Koyanagi-Harada disease and sympathetic ophthalmia. J Ophthalmic Inflamm Infect 2013;3:41.  Back to cited text no. 21
    


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