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Clinical characteristics of Fuchs’ Heterochromic Iridocyclitis in a tertiary medical center in Makkah region of Saudi Arabia: A retrospective study
Journal of Taibah University Medical Sciences (2014) 9(1), 65–68
Taibah University
Journal of Taibah University Medical Sciences www.sciencedirect.com
Clinical Study
Clinical characteristics of Fuchs’ Heterochromic Iridocyclitis in a tertiary medical center in Makkah region of Saudi Arabia: A retrospective study Ahmed M. Bawazeer, FRCSC Faculty of Medicine, King Abdulaziz University, Jeddah, Kingdom of Saudi Arabia Received 31 March 2013; revised 1 June 2013; accepted 3 June 2013
ﺍﻋﺘﺎﻡ ﻋﺪﺳﺔ ﺍﻟﻌﻴﻦ ﻟﺠﻤﻴﻊ ﺍﻟﻤﺮﺿﻰ .ﻭﻛﺎﻥ ﺃﻓﻀﻞ ﺗﺼﺤﻴﺢ ﻟﺤﺪﺓ ﺍﻟﺒﺼﺮ ﺃﻓﻀﻞ ﻣﻦ 0.5ﻋﻨﺪ (%63.2) 19/12ﻣﻦ ﺍﻟﻤﺮﺿﻰ ﻋﻨﺪ ﺍﻟﻤﺮﺍﺟﻌﺔ ﺍﻟﻨﻬﺎﺋﻴﺔ. ﺍﻻﺳﺘﻨﺘﺎﺟﺎﺕ :ﻳﻘﻞ ﻟﺪﻯ ﻣﺮﺿﺎﻧﺎ ﺗﻐﻴﺮ ﺍﻟﻠﻮﻥ ﻭﺍﻟﻌﻘﻴﺪﺍﺕ ﺍﻟﻘﺰﺣﻴﺔ .ﻣﻦ ﺍﻟﻤﻤﻜﻦ ﺃﻥ ﻳﺆﺩﻱ ﻭﺟﻮﺩ ﺿﻤﻮﺭ ﺍﻟﻘﺰﺣﻴﺔ ﺍﻟﺪﻗﻴﻖ ﻣﻊ ﺍﻟﺘﺮﺳﺒﺎﺕ ﺍﻟﻘﺮﻧﻴﺔ ﺍﻟﺪﻗﻴﻘﺔ ﻣﻊ ﺍﻟﺘﻬﺎﺏ ﺑﺴﻴﻂ ﺟﺪﺍ ﻓﻲ ﺗﺠﻮﻳﻒ ﺍﻟﻌﻴﻦ ﺍﻷﻣﺎﻣﻲ )>½ ﺧﻼﻳﺎ ﻭ >½ ﺗﻮﻫﺞ( ،ﺑﺎﻹﺿﺎﻓﺔ ﺇﻟﻰ ﺧﻼﻳﺎ ﺩﻗﻴﻘﺔ ﻭﺭﻛﺎﻡ ﻓﻲ ﺍﻟﺰﺟﺎﺟﻲ ﺇﻟﻰ ﺗﺸﺨﻴﺺ ﻣﺘﻼﺯﻣﺔ "ﻓﺘﺶ" ﻻﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﺍﻟﻤﺘﻐﻴﺮ ﺍﻟﻠﻮﻥ ﻓﻲ ﻣﺠﺘﻤﻌﻨﺎ. ﺍﻟﻜﻠﻤﺎﺕ ﺍﻟﻤﻔﺘﺎﺣﻴﺔ :ﻣﺘﻼﺯﻣﺔ ﻓﺘﺶ ﻻﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﻣﺘﻐﻴﺮﺓ ﺍﻟﻠﻮﻥ; ﺍﻟﺸﻌﺐ ﺍﻟﺴﻌﻮﺩﻱ; ﺍﻟﺘﻬﺎﺏ ﺍﻟﻘﺰﺣﻴﺔ Abstract ’Objectives: To characterize the clinical features of Fuchs Heterochromic Iridocyclitis in a Saudi population. Methods: Retrospective analysis of the records of the consecutive patients presented to the uveitis clinic, Magrabi Eye and Ear Hospital, Jeddah, Saudi Arabia, between 2001and 2011.
ﺍﻟﻤﻠﺨﺺ ﻫﺪﻑ ﺍﻟﺒﺤﺚ :ﻭﺻﻒ ﺍﻟﻤﻈﺎﻫﺮ ﺍﻟﺴﺮﻳﺮﻳﺔ ﻟﻤﺘﻼﺯﻣﺔ "ﻓﺘﺶ" ﻻﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﻣﺘﻐﻴﺮﺓ ﺍﻟﻠﻮﻥ ﻓﻲ ﺍﻟﻤﺠﺘﻤﻊ ﺍﻟﺴﻌﻮﺩﻱ. ﻃﺮﻕ ﺍﻟﺒﺤﺚ :ﺃﺟﺮﻳﺖ ﻫﺬﻩ ﺍﻟﺪﺭﺍﺳﺔ ﺑﺄﺛﺮ ﺭﺟﻌﻲ ﺑﻌﺪ ﺗﺤﻠﻴﻞ ﻣﻠﻔﺎﺕ ﺍﻟﻤﺮﺿﻰ ﺍﻟﻤﺮﺍﺟﻌﻴﻦ ﻟﻌﻴﺎﺩﺓ ﺍﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﻋﻠﻰ ﺍﻟﺘﻮﺍﻟﻲ ﻓﻲ ﻣﺴﺘﺸﻔﻰ ﺍﻟﻤﻐﺮﺑﻲ ﻟﻠﻌﻴﻮﻥ ﻭﺍﻷﺫﻥ، ﺟﺪﺓ ،ﺍﻟﻤﻤﻠﻜﺔ ﺍﻟﻌﺮﺑﻴﺔ ﺍﻟﺴﻌﻮﺩﻳﺔ ،ﺑﻴﻦ ﻋﺎﻣﻲ 2001ﻡ ﻭ 2011ﻡ. ﺍﻟﻨﺘﺎﺋﺞ :ﺗﻢ ﺇﺩﺭﺍﺝ 21ﻋﻴﻨﺎ ﻟﻌﺪﺩ 19ﻣﺮﻳﻀﺎ ﻳﻌﺎﻧﻮﻥ ﻣﻦ ﻣﺘﻼﺯﻣﺔ "ﻓﺘﺶ" ﻻﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﻣﺘﻐﻴﺮﺓ ﺍﻟﻠﻮﻥ ﺍﻟﺬﻳﻦ ﺃﻛﻤﻠﻮﺍ 6ﺃﺷﻬﺮ ﻋﻠﻰ ﺍﻷﻗﻞ ﻣﻦ ﺍﻟﻤﺘﺎﺑﻌﺔ .ﻭﻛﺎﻥ ﻣﺘﻮﺳﻂ ﻓﺘﺮﺓ ﺍﻟﻤﺮﺍﺟﻌﺔ ) 13,35 25ﺍﻟﻤﺪﻯ (48 – 6ﺷﻬﺮﺍ .ﺃﻏﻠﺒﻬﻢ ﻣﻦ ﺍﻟﺬﻛﻮﺭ )،19/13 .(% 68.3ﻛﻤﺎ ﺃﻥ ﺃﻏﻠﺒﻬﻢ ﻳﻌﺎﻧﻲ ﻣﻦ ﺇﺻﺎﺑﺔ ﺃﺣﺎﺩﻳﺔ ) .(% 89.5 ,19/17ﻭﻛﺎﻥ ﺍﻟﻌﻤﺮ ﻋﻨﺪ ﺍﻹﺻﺎﺑﺔ ) 11 36.2ﺍﻟﻤﺪﻯ (59 – 18ﻋﺎﻣﺎ .ﺗﻐﻴﺮ ﻟﻮﻥ ﺍﻟﻌﻨﺒﺔ ﻟﺪﻯ (19/6) % 31.6ﻣﻦ ﺍﻟﻤﺮﺿﻰ .ﻭﺟﺪ ﻟﺪﻯ ﺟﻤﻴﻊ ﺍﻟﻤﺮﺿﻰ ﺗﺮﺳﺒﺎﺕ ﻧﺠﻤﻴﺔ ﺧﻴﻄﻴﺔ ﺩﻗﻴﻘﺔ ﻓﻲ ﺍﻟﻘﺮﻧﻴﺔ ،ﻭﺃﻏﻠﺒﻬﻢ ) (%57.9ﻭﺟﺪ ﻟﺪﻳﻪ ﺍﻟﺘﻬﺎﺏ ﺧﻔﻴﻒ ﺑﺘﺠﻮﻳﻒ ﺍﻟﻌﻴﻦ ﺍﻷﻣﺎﻣﻲ )>½ ﺧﻼﻳﺎ ﻭ >½ ﺗﻮﻫﺞ( .ﻭﺷﻮﻫﺪ ﺿﻤﻮﺭ ﺍﻟﻘﺰﺣﻴﺔ ﻟﺪﻯ ﺍﻟﻐﺎﻟﺒﻴﺔ )/15 .(%78.9 ،19ﻛﻤﺎ ﻇﻬﺮ ﻟﺪﻯ ﺟﻤﻴﻊ ﺍﻟﻤﺮﺿﻰ ﺧﻼﻳﺎ ﺯﺟﺎﺟﻴﺔ ﺩﻗﻴﻘﺔ ﺑﺎﻹﺿﺎﻓﺔ ﺇﻟﻰ ﺭﻛﺎﻡ ﺯﺟﺎﺟﻲ .ﺑﻴﻨﻤﺎ ﻟﻢ ﻳﻈﻬﺮ ﻟﺪﻯ ﻏﺎﻟﺒﻴﺔ ﺍﻟﻤﺮﺿﻰ ) (% 78.9–19/15ﻋﻘﻴﺪﺍﺕ ﺍﻟﻘﺰﺣﻴﺔ .ﻭﺷﻮﻫﺪﺕ ﻋﻘﻴﺪﺍﺕ ﻛﻮﻳﺐ ﻋﻨﺪ ) (% 15.8 ،19/3ﻣﻦ ﺍﻟﻤﺮﺿﻰ. ﻭﻟﻮﺣﻈﺖ ﺍﻟﺘﺼﺎﻗﺎﺕ ﺳﻄﺤﻴﺔ ﺃﻣﺎﻣﻴﺔ ﻟﺪﻯ 3ﻣﺮﺿﻰ ) (%15.8ﻭﻋﺎﻧﻰ 2ﻣﻨﻬﻢ ﻣﻦ ﺍﺭﺗﻔﺎﻉ ﺍﻟﻀﻐﻂ ﺩﺍﺧﻞ ﺍﻟﻌﻴﻦ ﺍﻟﺬﻱ ﺍﺳﺘﺠﺎﺏ ﻟﻠﻌﻼﺟﺎﺕ ﺍﻟﻤﻀﺎﺩﺓ ﻟﻠﺠﻠﻮﻛﻮﻣﺎ .ﻭﺣﺼﻞ
Corresponding address: Chairman & Associate Professor, King Abdulaziz University, Faculty of Medicine, P.O. Box 80215, Jeddah – Zip code: 21589, Kingdom of Saudi Arabia. Tel.: +966 505353015; fax: +966 22574294. )E-mail: [email protected] (A. Bawazeer Peer review under responsibility of Taibah University.
Production and hosting by Elsevier 1658-3612 Ó 2014 Taibah University. Production and hosting by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jtumed.2013.06.003
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A.M. Bawazeer Results: We enrolled 21 eyes of 19 patients with the diagnosis of Fuch’s Heterochromic Iridocyclitis who completed a minimum of 6 months follow up. The mean follow up was 25 13.35 (range 6–48) months. Males predominated (13/ 19, 68.3%). Majority (17/19, 89.5%) had unilateral presentation. The age at presentation was 36.2 11 (range 18–59) years. 31.6% (6/19) showed heterochromia. All patients (100%) showed fine stellate filamentary keratic precipitates and majority (57.9%) showed mild (<1/2 cells and <1/2 flare) anterior chamber inflammation. Iris atrophy was seen in majority (15/19, 78.9%) of patients. All (100%) showed fine vitreous cells and vitreous debris. In majority of patients (15/19, 78.9%) Iris nodules were absent. Koeppe nodules were seen in 15.8% (3/19) patients. Peripheral anterior synechiae was noted in 3 (15.8%) patients and 2 of them had elevated intraocular pressure which responded to anti glaucoma treatment. All patients had developed cataracts. Best corrected visual acuity was better than 0.5 in 12/19 (63.2%) of patients at the final follow up. Conclusion: Our patients had less heterochromia and Iris nodules. Subtle iris atrophy with fine keratic precipitates and very mild anterior chamber inflammation (<1/2 cells, <1/2 flare) along with fine vitreous cells and debris could lead to the diagnosis of Fuch’s Heterochromic Iridocyclitis in our population. Keywords: Fuch’s Heterochromic Iridocyclitis; Saudi population; Uveitis Ó 2014 Taibah University. Production and hosting by Elsevier Ltd. All rights reserved.
Introduction Fuchs’ Heterochromic Iridocyclitis (FHI) is a chronic-low grade anterior uveitis characterized by iris heterochromia. The uveitis usually occurs with few ocular symptoms and not related to any systemic disease. The diagnosis of FHI is based on the criteria of Kimura et al.1 which includes small, white, diffuse stellate keratic precipitates on the corneal endothelium, mild anterior chamber cells and flare, lack of irido-capsular posterior synechiae, vitreous disorders such as floaters, vitreous debris, and vitreous cells (63–88% of cases), glaucoma (9–59% of cases), and iris atrophy with or without heterochromia. Previous studies have suggested variations in the clinical spectrum of FHI in different populations.2–5 The etiology of FHI remains elusive. Ernst Fuchs, who firstly described this disease in 1906, assumed that this syndrome was caused by a noxious factor of unknown origin.6 Since then, many theories (genetic, sympathetic, Immunological, vascular theories) and associations with toxoplasma were proposed. Recent studies have shown evidence for viral (rubella) etiology in at least some cases of FHI.9–11 Vaccination programs and variable sero-prevalence of infections in different populations have been suggested to affect disease prevalence and expression.8 Comparison of clinical patterns may have
implications for future studies that investigate etiology of FHI in different population. The purpose of the present study was to report the clinical features of FHI in our part of the world. Materials and Methods Retrospective review of the clinical records of the patients with FHI who attended the Uveitis clinic of Magrabi Eye and Ear Hospital, Jeddah, between 2001 and 2011 was done. The diagnosis of FHI was based on the clinical criteria of Kimura.1 Other causes of infectious or non infectious uveitis were excluded in our patients. Diagnostic investigations including C Reactive Protein (CRP), erythrocyte sedimentation rate, complete blood count, tuberculin skin testing, chest radiography, angiotensin-converting enzyme assay, syphilis serology (VDRL and TPHA), and Human Leukocyte Antigen B27 (HLA B27) were ordered. For all cases a detailed medical and ocular history were obtained. At the initial visit, every patient was checked for best-corrected visual acuity (VA), slit-lamp biomicroscopy, goldmann applanation tonometry, indirect ophthalmoscopy, and gonioscopy. The ora serrata and peripheral retina were examined to rule out snow banking in eyes with significant vitreous inflammation. Fluorescein angiography (FA) was performed in selected cases to exclude the possibilities of retinal vasculitis and macular edema. Results We found 25 patients of FHI among 587 patients who attended our uveitis clinic in Magrabi Eye and Ear Hospital. Among them, we included 19 patients who completed at least 6 months follow up. We had 13 (68.3%) males and 6 (31.6%) females. Unilateral affection was present in 17 (89.5%) patients and bilateral in two (10.5%) cases. The mean follow up was 25 13.35 (range 6–48) months. The age of the patients at the time of presentation varied from 18 to 59 years with a mean of 36.2 11 years. Heterochromia was present in 6 (31.6%) patients. Posterior subcapsular cortical cataract was present in all patients (100%). Anterior chamber examination showed fine keratic precipitates (KPs) and <+1/ 2 cells and <1/2 flare in all the patients (100%). Peripheral anterior synechiae (PAS) was present in 3 (15.8%) patients and 2 (10.5%) of them had elevated pressure that required medications and were controlled. No retinal lesions or any scars of old toxoplasmosis were seen in any of our patients, while fine vitreous cells or debris was seen in all patients (100%). A clinical diagnosis of FHI was made or confirmed at the initial visit by uveitis specialist (author). The most frequent presenting symptom was visual blurring (100%). Six patients (31.6%) were aware of the presence of heterochromia. Best Corrected Visual Acuity (BCVA) at the last follow up was 0.5 or better in 12 patients (63.2%), and less than 0.1 in 7 eyes (36.81%). Causes of diminished BCVA were cataract in all cases. Ten (52.6%) patients required no medications at the time of presentation while 9 (47.4%) patients were on topical non steroidal medications with or without combined topical steroids antibiotics eye drops. Ocular findings are shown in Table 1 and Figure 1.
Clinical characteristics of Fuchs’ Heterochromic Iridocyclitis Table 1: Clinical characteristics of patients presented with Fuch’s heterochromia Iridocyclitis. Sex Female Male Age Range Mean SD OD/OS OD OS OU Heterochromia Absent Present Iris atrophy Absent Present Iris nodules Absent Busaca Koeppe Stellate KPs Present with filaments AC reaction +1 cells and flare +1/2 cells and flare +2 cells and flare Occasional cells and flare Rare cells and flares Iris vessels Absent Present Angle vessels and PAS Absent Present Cataract Vitreous cells and debris
No.
%
6 13
31.6 68.4 18–59 years 36.32 11.828
7 10 2
36.8 52.6 10.5
13 6
68.4 31.6
4 15
21.1 78.9
15 1 3
78.9 5.3 15.8
19
100.0
1 11 1 3 3
5.3 57.9 5.3 15.8 15.8
12 7
63.2 36.8
16 3 19 19
84.2 15.8 100 100
Discussion The FHI is a relatively rare condition. The prevalence of FHI in uveitis population varies from 1.2% to 4.5% in various published studies. Recently, we found out 4.3% of prevalence of FHI among total uveitis cases and 7.4% among anterior uveitis cases.12 Other studies from Saudi Arabia also reported the prevalence that varies from 2% to 4%.13–15 The mean age in our series was 36.2 years. In other series the mean age was from 29.5 to 40.2–5 The FHI is usually unilateral. In our study majority 17/19 (89.4%) patients had unilateral uveitis. The KPs in FHI have been classically described as having a stellate morphology with fibrillary extensions2–5. Small and medium-sized round non pigmented KPs were more common in our study. Chee and Jap7 reported the occurrence of medium sized nodular endothelial deposits in eyes with FHI that had cytomegalovirus (CMV) antigen in the aqueous humor compared to eyes with CMV-negative FHI (60% vs 9.5%). They postulated that CMV-infected endothelial cells might be responsible for the nodular endothelial lesions. As aqueous
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humor analysis was not done in our study, this data could not be confirmed. Heterochromia was absent in majority (13/19, 68%) of our patients. Heterochromia is reported to be less common in FHI patients with dark brown eyes.2–5 All of our patients had brown eyes. Detection of subtle changes on the surface of the iris, i.e., blunting of crypts, is more helpful for the diagnosis of FUS in dark irides. We also found subtle blunting of iris crypts in all our patients. Rothova and associates16 suggested that the presence of unilateral multiple iris nodules without the formation of synechiae or heterochromia might be important for the diagnosis of FHI, especially in dark iris. Iris nodules were absent in majority (15/19, 78.9%) of our patients. Koeppe nodules were more frequently seen than Busacca nodules in our study, consistent with previous reports.2,5 Jones17 suggested that iris nodules were most often found in eyes without iris atrophy or cataract during the early stages of the disease. Majority of our patients (15/19, 79%) had iris atrophy. In our study, we observed iris nodules in eyes with either cataract or pseudophakia. The presence of diffuse vitreous cells and debris adherent to the vitreous fibrils often lead to a misdiagnosis in patients with FHI. The presence of a healthy foveal reflex and the absence of other inflammatory findings in the fundus should alert clinicians to search for FHI in patients with uveitis. In this series, vitreous cells and fine debris were present in all (100%) patients. Cataract is the most common complication of FHI. The estimated risk of cataract development was 56% at 8 years in patients who did not receive topical corticosteroids during follow-up. The high prevalence of cataract at presentation implies a longer duration of disease.2–5 In our study, cataract was present in all cases and this could be due to the longer duration of the disease. Al Mansour et al.,18 recently found out that, a shorter interval between onset of symptoms and presentation, better initial visual acuity, and no glaucoma surgery was significantly associated with better final visual acuity in 166 patients of FHI (1983–2005) in a tertiary center from the Riyadh region of Saudi Arabia. We had lesser number of patients and lesser follow up. In our study, majority (63%) had better than 0.5 visual acuity at the final follow up. We noted cataract in all our patients. Two patients had glaucoma which was able to be controlled by medications. Our study suffers from the drawbacks inherent to a retrospective study. We have a less number of patients, but still, the prevalence of FHI in our study is the highest (4.3%) among the studies published from Saudi Arabia.13–15 The aqueous fluid analysis was not done in our patients which could have given new insights into the etiology of FHI in our population. In conclusion, by comparing this data with other series, it was noted that fine keratic precipitates and subtle iris atrophy were more common in our patients while heterochromia and iris nodules were less frequent. Other clinical features such as subtle iris changes and vitreous opacities in the absence of macular edema were more often useful clues to the diagnosis than heterochromia in Saudi population. The risk of cataract development was much higher than the risk of glaucoma in patients who were not exposed to the side effects of corticosteroids. Analysis of aqueous humor in future studies may reveal whether Rubella virus or CMV or another causative
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A.M. Bawazeer
Figure 1: Presentation of clinical signs in patients with Fuch’s heterochromia uveitis.
agent is predominantly responsible for FHI in Saudi patients and may explain the variable clinical characteristics in this study. Conflict of interest None declared. Acknowledgments I hereby express my heartfelt gratitude to Dr. S.H.M. Nizamuddin, Vitreo-Retina Consultant, King Abdulaziz University Hospital and Dr May Mulham Al Baroudi, Resident in Ophthalmology for their help in editing the manuscript. References 1. Kimura SJ, Hogan MJ, Thygeson P. Fuchs syndrome of Heterochromic cyclitis. Arch Ophthalmol 1955; 54: 179–186. 2. Yang P, Fang W, Jin H, Li B, Chen X, Kijlstra A. Clinical features of Chinese patients with Fuchs’ syndrome. Ophthalmology 2006; 113: 473–480. 3. Arellanes-Garcia L, Preciado-Delgadillo MDC, Recillas-Gispert C. Fuchs’ heterochromic iridocyclitis: clinical manifestations in dark-eyed Mexican patients. Ocul Immunol Inflamm 2002; 10: 125–131. 4. Norrsell K, SjIˆdell L. Fuchs’ heterochromic uveitis: a longitudinal clinical study. Acta Ophthalmol 2008; 86: 58–64. 5. Mohamed Q, Zamir E. Update on Fuchs’ uveitis syndrome. Curr Opin Ophthalmol 2005; 16: 356–363. 6. Foster CS, Vitale AT. Diagnosis and treatment of uveitis. 2nd ed. New Delhi: Jaypee Brothers; 2013, p. 925–934 chapter 62.
7. Chee SP, Jap A. Presumed Fuchs heterochromic iridocyclitis and Posner-Schlossman syndrome: comparison of cytomegaloviruspositive and negative eyes. Am J Ophthalmol 2008; 146: 883–889. 8. Birnbaum AD, Tessler HH, Schultz KL, et al. Epidemiologic relationship between Fuchs heterochromic iridocyclitis and the United States rubella vaccination program. Am J Ophthalmol 2007; 144: 424–428. 9. Quentin CD, Reiber H. Fuchs’heterochromic cyclitis: rubella virus antibodies and genome in aqueous humor. Am J Ophthalmol 2004; 138: 46–54. 10. De Groot-Mijnes JDF, de Visser L, Rothova A, Schuller M, van Loon AM, Weersink AJL. Rubella virus is associated with Fuchs heterochromic iridocyclitis. Am J Ophthalmol 2006; 141: 212–214. 11. De Visser L, Braakenburg A, Rothova A, de Boer JH. Rubella virus–associated uveitis: clinical manifestations and visual prognosis. Am J Ophthalmol 2008; 146: 292–297. 12. Nizamuddin SHM, Bawazeer AM. Causes of uveitis in a tertiary center in Western Saudi Arabia: a retrospective study. Saudi Med J 2013; 34(4): 179–187. 13. Islam SM, Tabbara KF. Causes of uveitis at The Eye Centre in Saudi Arabia: a retrospective review. Ophthalmic Epidemiol 2002; 9(4): 239–249. 14. Hamade IH, Elkum N, Tabbara KF. Causes of uveitis at a referral center in Saudi Arabia. Ocul Immunol Inflamm 2009; 17(1): 11–16. 15. Al-Mezaine HS, Kangave D, Abu El-Asrar AM. Patterns of uveitis in patients admitted to a University Hospital in Riyadh, Saudi Arabia. Ocul Immunol Inflamm 2010; 18(6): 424–431. 16. Rothova A, La Hey E, Baarsma GS, Breebaart AC. Iris nodules in Fuchs’ heterochromic uveitis. Am J Ophthalmol 1994; 118: 338–342. 17. Jones NP. Fuchs’ heterochromic uveitis: an update. Surv Ophthalmol 1993; 37: 253–272. 18. Al-Mansour YS, Al-Rajhi AA, Al-Dhibi H, Abu El-Asrar AM. Clinical features and prognostic factors in Fuchs’ uveitis. Int Ophthalmol 2010; 30(5): 501–509.
Taibah University
Journal of Taibah University Medical Sciences www.sciencedirect.com
Clinical Study
Clinical characteristics of Fuchs’ Heterochromic Iridocyclitis in a tertiary medical center in Makkah region of Saudi Arabia: A retrospective study Ahmed M. Bawazeer, FRCSC Faculty of Medicine, King Abdulaziz University, Jeddah, Kingdom of Saudi Arabia Received 31 March 2013; revised 1 June 2013; accepted 3 June 2013
ﺍﻋﺘﺎﻡ ﻋﺪﺳﺔ ﺍﻟﻌﻴﻦ ﻟﺠﻤﻴﻊ ﺍﻟﻤﺮﺿﻰ .ﻭﻛﺎﻥ ﺃﻓﻀﻞ ﺗﺼﺤﻴﺢ ﻟﺤﺪﺓ ﺍﻟﺒﺼﺮ ﺃﻓﻀﻞ ﻣﻦ 0.5ﻋﻨﺪ (%63.2) 19/12ﻣﻦ ﺍﻟﻤﺮﺿﻰ ﻋﻨﺪ ﺍﻟﻤﺮﺍﺟﻌﺔ ﺍﻟﻨﻬﺎﺋﻴﺔ. ﺍﻻﺳﺘﻨﺘﺎﺟﺎﺕ :ﻳﻘﻞ ﻟﺪﻯ ﻣﺮﺿﺎﻧﺎ ﺗﻐﻴﺮ ﺍﻟﻠﻮﻥ ﻭﺍﻟﻌﻘﻴﺪﺍﺕ ﺍﻟﻘﺰﺣﻴﺔ .ﻣﻦ ﺍﻟﻤﻤﻜﻦ ﺃﻥ ﻳﺆﺩﻱ ﻭﺟﻮﺩ ﺿﻤﻮﺭ ﺍﻟﻘﺰﺣﻴﺔ ﺍﻟﺪﻗﻴﻖ ﻣﻊ ﺍﻟﺘﺮﺳﺒﺎﺕ ﺍﻟﻘﺮﻧﻴﺔ ﺍﻟﺪﻗﻴﻘﺔ ﻣﻊ ﺍﻟﺘﻬﺎﺏ ﺑﺴﻴﻂ ﺟﺪﺍ ﻓﻲ ﺗﺠﻮﻳﻒ ﺍﻟﻌﻴﻦ ﺍﻷﻣﺎﻣﻲ )>½ ﺧﻼﻳﺎ ﻭ >½ ﺗﻮﻫﺞ( ،ﺑﺎﻹﺿﺎﻓﺔ ﺇﻟﻰ ﺧﻼﻳﺎ ﺩﻗﻴﻘﺔ ﻭﺭﻛﺎﻡ ﻓﻲ ﺍﻟﺰﺟﺎﺟﻲ ﺇﻟﻰ ﺗﺸﺨﻴﺺ ﻣﺘﻼﺯﻣﺔ "ﻓﺘﺶ" ﻻﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﺍﻟﻤﺘﻐﻴﺮ ﺍﻟﻠﻮﻥ ﻓﻲ ﻣﺠﺘﻤﻌﻨﺎ. ﺍﻟﻜﻠﻤﺎﺕ ﺍﻟﻤﻔﺘﺎﺣﻴﺔ :ﻣﺘﻼﺯﻣﺔ ﻓﺘﺶ ﻻﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﻣﺘﻐﻴﺮﺓ ﺍﻟﻠﻮﻥ; ﺍﻟﺸﻌﺐ ﺍﻟﺴﻌﻮﺩﻱ; ﺍﻟﺘﻬﺎﺏ ﺍﻟﻘﺰﺣﻴﺔ Abstract ’Objectives: To characterize the clinical features of Fuchs Heterochromic Iridocyclitis in a Saudi population. Methods: Retrospective analysis of the records of the consecutive patients presented to the uveitis clinic, Magrabi Eye and Ear Hospital, Jeddah, Saudi Arabia, between 2001and 2011.
ﺍﻟﻤﻠﺨﺺ ﻫﺪﻑ ﺍﻟﺒﺤﺚ :ﻭﺻﻒ ﺍﻟﻤﻈﺎﻫﺮ ﺍﻟﺴﺮﻳﺮﻳﺔ ﻟﻤﺘﻼﺯﻣﺔ "ﻓﺘﺶ" ﻻﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﻣﺘﻐﻴﺮﺓ ﺍﻟﻠﻮﻥ ﻓﻲ ﺍﻟﻤﺠﺘﻤﻊ ﺍﻟﺴﻌﻮﺩﻱ. ﻃﺮﻕ ﺍﻟﺒﺤﺚ :ﺃﺟﺮﻳﺖ ﻫﺬﻩ ﺍﻟﺪﺭﺍﺳﺔ ﺑﺄﺛﺮ ﺭﺟﻌﻲ ﺑﻌﺪ ﺗﺤﻠﻴﻞ ﻣﻠﻔﺎﺕ ﺍﻟﻤﺮﺿﻰ ﺍﻟﻤﺮﺍﺟﻌﻴﻦ ﻟﻌﻴﺎﺩﺓ ﺍﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﻋﻠﻰ ﺍﻟﺘﻮﺍﻟﻲ ﻓﻲ ﻣﺴﺘﺸﻔﻰ ﺍﻟﻤﻐﺮﺑﻲ ﻟﻠﻌﻴﻮﻥ ﻭﺍﻷﺫﻥ، ﺟﺪﺓ ،ﺍﻟﻤﻤﻠﻜﺔ ﺍﻟﻌﺮﺑﻴﺔ ﺍﻟﺴﻌﻮﺩﻳﺔ ،ﺑﻴﻦ ﻋﺎﻣﻲ 2001ﻡ ﻭ 2011ﻡ. ﺍﻟﻨﺘﺎﺋﺞ :ﺗﻢ ﺇﺩﺭﺍﺝ 21ﻋﻴﻨﺎ ﻟﻌﺪﺩ 19ﻣﺮﻳﻀﺎ ﻳﻌﺎﻧﻮﻥ ﻣﻦ ﻣﺘﻼﺯﻣﺔ "ﻓﺘﺶ" ﻻﻟﺘﻬﺎﺏ ﺍﻟﻌﻨﺒﺔ ﻣﺘﻐﻴﺮﺓ ﺍﻟﻠﻮﻥ ﺍﻟﺬﻳﻦ ﺃﻛﻤﻠﻮﺍ 6ﺃﺷﻬﺮ ﻋﻠﻰ ﺍﻷﻗﻞ ﻣﻦ ﺍﻟﻤﺘﺎﺑﻌﺔ .ﻭﻛﺎﻥ ﻣﺘﻮﺳﻂ ﻓﺘﺮﺓ ﺍﻟﻤﺮﺍﺟﻌﺔ ) 13,35 25ﺍﻟﻤﺪﻯ (48 – 6ﺷﻬﺮﺍ .ﺃﻏﻠﺒﻬﻢ ﻣﻦ ﺍﻟﺬﻛﻮﺭ )،19/13 .(% 68.3ﻛﻤﺎ ﺃﻥ ﺃﻏﻠﺒﻬﻢ ﻳﻌﺎﻧﻲ ﻣﻦ ﺇﺻﺎﺑﺔ ﺃﺣﺎﺩﻳﺔ ) .(% 89.5 ,19/17ﻭﻛﺎﻥ ﺍﻟﻌﻤﺮ ﻋﻨﺪ ﺍﻹﺻﺎﺑﺔ ) 11 36.2ﺍﻟﻤﺪﻯ (59 – 18ﻋﺎﻣﺎ .ﺗﻐﻴﺮ ﻟﻮﻥ ﺍﻟﻌﻨﺒﺔ ﻟﺪﻯ (19/6) % 31.6ﻣﻦ ﺍﻟﻤﺮﺿﻰ .ﻭﺟﺪ ﻟﺪﻯ ﺟﻤﻴﻊ ﺍﻟﻤﺮﺿﻰ ﺗﺮﺳﺒﺎﺕ ﻧﺠﻤﻴﺔ ﺧﻴﻄﻴﺔ ﺩﻗﻴﻘﺔ ﻓﻲ ﺍﻟﻘﺮﻧﻴﺔ ،ﻭﺃﻏﻠﺒﻬﻢ ) (%57.9ﻭﺟﺪ ﻟﺪﻳﻪ ﺍﻟﺘﻬﺎﺏ ﺧﻔﻴﻒ ﺑﺘﺠﻮﻳﻒ ﺍﻟﻌﻴﻦ ﺍﻷﻣﺎﻣﻲ )>½ ﺧﻼﻳﺎ ﻭ >½ ﺗﻮﻫﺞ( .ﻭﺷﻮﻫﺪ ﺿﻤﻮﺭ ﺍﻟﻘﺰﺣﻴﺔ ﻟﺪﻯ ﺍﻟﻐﺎﻟﺒﻴﺔ )/15 .(%78.9 ،19ﻛﻤﺎ ﻇﻬﺮ ﻟﺪﻯ ﺟﻤﻴﻊ ﺍﻟﻤﺮﺿﻰ ﺧﻼﻳﺎ ﺯﺟﺎﺟﻴﺔ ﺩﻗﻴﻘﺔ ﺑﺎﻹﺿﺎﻓﺔ ﺇﻟﻰ ﺭﻛﺎﻡ ﺯﺟﺎﺟﻲ .ﺑﻴﻨﻤﺎ ﻟﻢ ﻳﻈﻬﺮ ﻟﺪﻯ ﻏﺎﻟﺒﻴﺔ ﺍﻟﻤﺮﺿﻰ ) (% 78.9–19/15ﻋﻘﻴﺪﺍﺕ ﺍﻟﻘﺰﺣﻴﺔ .ﻭﺷﻮﻫﺪﺕ ﻋﻘﻴﺪﺍﺕ ﻛﻮﻳﺐ ﻋﻨﺪ ) (% 15.8 ،19/3ﻣﻦ ﺍﻟﻤﺮﺿﻰ. ﻭﻟﻮﺣﻈﺖ ﺍﻟﺘﺼﺎﻗﺎﺕ ﺳﻄﺤﻴﺔ ﺃﻣﺎﻣﻴﺔ ﻟﺪﻯ 3ﻣﺮﺿﻰ ) (%15.8ﻭﻋﺎﻧﻰ 2ﻣﻨﻬﻢ ﻣﻦ ﺍﺭﺗﻔﺎﻉ ﺍﻟﻀﻐﻂ ﺩﺍﺧﻞ ﺍﻟﻌﻴﻦ ﺍﻟﺬﻱ ﺍﺳﺘﺠﺎﺏ ﻟﻠﻌﻼﺟﺎﺕ ﺍﻟﻤﻀﺎﺩﺓ ﻟﻠﺠﻠﻮﻛﻮﻣﺎ .ﻭﺣﺼﻞ
Corresponding address: Chairman & Associate Professor, King Abdulaziz University, Faculty of Medicine, P.O. Box 80215, Jeddah – Zip code: 21589, Kingdom of Saudi Arabia. Tel.: +966 505353015; fax: +966 22574294. )E-mail: [email protected] (A. Bawazeer Peer review under responsibility of Taibah University.
Production and hosting by Elsevier 1658-3612 Ó 2014 Taibah University. Production and hosting by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jtumed.2013.06.003
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A.M. Bawazeer Results: We enrolled 21 eyes of 19 patients with the diagnosis of Fuch’s Heterochromic Iridocyclitis who completed a minimum of 6 months follow up. The mean follow up was 25 13.35 (range 6–48) months. Males predominated (13/ 19, 68.3%). Majority (17/19, 89.5%) had unilateral presentation. The age at presentation was 36.2 11 (range 18–59) years. 31.6% (6/19) showed heterochromia. All patients (100%) showed fine stellate filamentary keratic precipitates and majority (57.9%) showed mild (<1/2 cells and <1/2 flare) anterior chamber inflammation. Iris atrophy was seen in majority (15/19, 78.9%) of patients. All (100%) showed fine vitreous cells and vitreous debris. In majority of patients (15/19, 78.9%) Iris nodules were absent. Koeppe nodules were seen in 15.8% (3/19) patients. Peripheral anterior synechiae was noted in 3 (15.8%) patients and 2 of them had elevated intraocular pressure which responded to anti glaucoma treatment. All patients had developed cataracts. Best corrected visual acuity was better than 0.5 in 12/19 (63.2%) of patients at the final follow up. Conclusion: Our patients had less heterochromia and Iris nodules. Subtle iris atrophy with fine keratic precipitates and very mild anterior chamber inflammation (<1/2 cells, <1/2 flare) along with fine vitreous cells and debris could lead to the diagnosis of Fuch’s Heterochromic Iridocyclitis in our population. Keywords: Fuch’s Heterochromic Iridocyclitis; Saudi population; Uveitis Ó 2014 Taibah University. Production and hosting by Elsevier Ltd. All rights reserved.
Introduction Fuchs’ Heterochromic Iridocyclitis (FHI) is a chronic-low grade anterior uveitis characterized by iris heterochromia. The uveitis usually occurs with few ocular symptoms and not related to any systemic disease. The diagnosis of FHI is based on the criteria of Kimura et al.1 which includes small, white, diffuse stellate keratic precipitates on the corneal endothelium, mild anterior chamber cells and flare, lack of irido-capsular posterior synechiae, vitreous disorders such as floaters, vitreous debris, and vitreous cells (63–88% of cases), glaucoma (9–59% of cases), and iris atrophy with or without heterochromia. Previous studies have suggested variations in the clinical spectrum of FHI in different populations.2–5 The etiology of FHI remains elusive. Ernst Fuchs, who firstly described this disease in 1906, assumed that this syndrome was caused by a noxious factor of unknown origin.6 Since then, many theories (genetic, sympathetic, Immunological, vascular theories) and associations with toxoplasma were proposed. Recent studies have shown evidence for viral (rubella) etiology in at least some cases of FHI.9–11 Vaccination programs and variable sero-prevalence of infections in different populations have been suggested to affect disease prevalence and expression.8 Comparison of clinical patterns may have
implications for future studies that investigate etiology of FHI in different population. The purpose of the present study was to report the clinical features of FHI in our part of the world. Materials and Methods Retrospective review of the clinical records of the patients with FHI who attended the Uveitis clinic of Magrabi Eye and Ear Hospital, Jeddah, between 2001 and 2011 was done. The diagnosis of FHI was based on the clinical criteria of Kimura.1 Other causes of infectious or non infectious uveitis were excluded in our patients. Diagnostic investigations including C Reactive Protein (CRP), erythrocyte sedimentation rate, complete blood count, tuberculin skin testing, chest radiography, angiotensin-converting enzyme assay, syphilis serology (VDRL and TPHA), and Human Leukocyte Antigen B27 (HLA B27) were ordered. For all cases a detailed medical and ocular history were obtained. At the initial visit, every patient was checked for best-corrected visual acuity (VA), slit-lamp biomicroscopy, goldmann applanation tonometry, indirect ophthalmoscopy, and gonioscopy. The ora serrata and peripheral retina were examined to rule out snow banking in eyes with significant vitreous inflammation. Fluorescein angiography (FA) was performed in selected cases to exclude the possibilities of retinal vasculitis and macular edema. Results We found 25 patients of FHI among 587 patients who attended our uveitis clinic in Magrabi Eye and Ear Hospital. Among them, we included 19 patients who completed at least 6 months follow up. We had 13 (68.3%) males and 6 (31.6%) females. Unilateral affection was present in 17 (89.5%) patients and bilateral in two (10.5%) cases. The mean follow up was 25 13.35 (range 6–48) months. The age of the patients at the time of presentation varied from 18 to 59 years with a mean of 36.2 11 years. Heterochromia was present in 6 (31.6%) patients. Posterior subcapsular cortical cataract was present in all patients (100%). Anterior chamber examination showed fine keratic precipitates (KPs) and <+1/ 2 cells and <1/2 flare in all the patients (100%). Peripheral anterior synechiae (PAS) was present in 3 (15.8%) patients and 2 (10.5%) of them had elevated pressure that required medications and were controlled. No retinal lesions or any scars of old toxoplasmosis were seen in any of our patients, while fine vitreous cells or debris was seen in all patients (100%). A clinical diagnosis of FHI was made or confirmed at the initial visit by uveitis specialist (author). The most frequent presenting symptom was visual blurring (100%). Six patients (31.6%) were aware of the presence of heterochromia. Best Corrected Visual Acuity (BCVA) at the last follow up was 0.5 or better in 12 patients (63.2%), and less than 0.1 in 7 eyes (36.81%). Causes of diminished BCVA were cataract in all cases. Ten (52.6%) patients required no medications at the time of presentation while 9 (47.4%) patients were on topical non steroidal medications with or without combined topical steroids antibiotics eye drops. Ocular findings are shown in Table 1 and Figure 1.
Clinical characteristics of Fuchs’ Heterochromic Iridocyclitis Table 1: Clinical characteristics of patients presented with Fuch’s heterochromia Iridocyclitis. Sex Female Male Age Range Mean SD OD/OS OD OS OU Heterochromia Absent Present Iris atrophy Absent Present Iris nodules Absent Busaca Koeppe Stellate KPs Present with filaments AC reaction +1 cells and flare +1/2 cells and flare +2 cells and flare Occasional cells and flare Rare cells and flares Iris vessels Absent Present Angle vessels and PAS Absent Present Cataract Vitreous cells and debris
No.
%
6 13
31.6 68.4 18–59 years 36.32 11.828
7 10 2
36.8 52.6 10.5
13 6
68.4 31.6
4 15
21.1 78.9
15 1 3
78.9 5.3 15.8
19
100.0
1 11 1 3 3
5.3 57.9 5.3 15.8 15.8
12 7
63.2 36.8
16 3 19 19
84.2 15.8 100 100
Discussion The FHI is a relatively rare condition. The prevalence of FHI in uveitis population varies from 1.2% to 4.5% in various published studies. Recently, we found out 4.3% of prevalence of FHI among total uveitis cases and 7.4% among anterior uveitis cases.12 Other studies from Saudi Arabia also reported the prevalence that varies from 2% to 4%.13–15 The mean age in our series was 36.2 years. In other series the mean age was from 29.5 to 40.2–5 The FHI is usually unilateral. In our study majority 17/19 (89.4%) patients had unilateral uveitis. The KPs in FHI have been classically described as having a stellate morphology with fibrillary extensions2–5. Small and medium-sized round non pigmented KPs were more common in our study. Chee and Jap7 reported the occurrence of medium sized nodular endothelial deposits in eyes with FHI that had cytomegalovirus (CMV) antigen in the aqueous humor compared to eyes with CMV-negative FHI (60% vs 9.5%). They postulated that CMV-infected endothelial cells might be responsible for the nodular endothelial lesions. As aqueous
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humor analysis was not done in our study, this data could not be confirmed. Heterochromia was absent in majority (13/19, 68%) of our patients. Heterochromia is reported to be less common in FHI patients with dark brown eyes.2–5 All of our patients had brown eyes. Detection of subtle changes on the surface of the iris, i.e., blunting of crypts, is more helpful for the diagnosis of FUS in dark irides. We also found subtle blunting of iris crypts in all our patients. Rothova and associates16 suggested that the presence of unilateral multiple iris nodules without the formation of synechiae or heterochromia might be important for the diagnosis of FHI, especially in dark iris. Iris nodules were absent in majority (15/19, 78.9%) of our patients. Koeppe nodules were more frequently seen than Busacca nodules in our study, consistent with previous reports.2,5 Jones17 suggested that iris nodules were most often found in eyes without iris atrophy or cataract during the early stages of the disease. Majority of our patients (15/19, 79%) had iris atrophy. In our study, we observed iris nodules in eyes with either cataract or pseudophakia. The presence of diffuse vitreous cells and debris adherent to the vitreous fibrils often lead to a misdiagnosis in patients with FHI. The presence of a healthy foveal reflex and the absence of other inflammatory findings in the fundus should alert clinicians to search for FHI in patients with uveitis. In this series, vitreous cells and fine debris were present in all (100%) patients. Cataract is the most common complication of FHI. The estimated risk of cataract development was 56% at 8 years in patients who did not receive topical corticosteroids during follow-up. The high prevalence of cataract at presentation implies a longer duration of disease.2–5 In our study, cataract was present in all cases and this could be due to the longer duration of the disease. Al Mansour et al.,18 recently found out that, a shorter interval between onset of symptoms and presentation, better initial visual acuity, and no glaucoma surgery was significantly associated with better final visual acuity in 166 patients of FHI (1983–2005) in a tertiary center from the Riyadh region of Saudi Arabia. We had lesser number of patients and lesser follow up. In our study, majority (63%) had better than 0.5 visual acuity at the final follow up. We noted cataract in all our patients. Two patients had glaucoma which was able to be controlled by medications. Our study suffers from the drawbacks inherent to a retrospective study. We have a less number of patients, but still, the prevalence of FHI in our study is the highest (4.3%) among the studies published from Saudi Arabia.13–15 The aqueous fluid analysis was not done in our patients which could have given new insights into the etiology of FHI in our population. In conclusion, by comparing this data with other series, it was noted that fine keratic precipitates and subtle iris atrophy were more common in our patients while heterochromia and iris nodules were less frequent. Other clinical features such as subtle iris changes and vitreous opacities in the absence of macular edema were more often useful clues to the diagnosis than heterochromia in Saudi population. The risk of cataract development was much higher than the risk of glaucoma in patients who were not exposed to the side effects of corticosteroids. Analysis of aqueous humor in future studies may reveal whether Rubella virus or CMV or another causative
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A.M. Bawazeer
Figure 1: Presentation of clinical signs in patients with Fuch’s heterochromia uveitis.
agent is predominantly responsible for FHI in Saudi patients and may explain the variable clinical characteristics in this study. Conflict of interest None declared. Acknowledgments I hereby express my heartfelt gratitude to Dr. S.H.M. Nizamuddin, Vitreo-Retina Consultant, King Abdulaziz University Hospital and Dr May Mulham Al Baroudi, Resident in Ophthalmology for their help in editing the manuscript. References 1. Kimura SJ, Hogan MJ, Thygeson P. Fuchs syndrome of Heterochromic cyclitis. Arch Ophthalmol 1955; 54: 179–186. 2. Yang P, Fang W, Jin H, Li B, Chen X, Kijlstra A. Clinical features of Chinese patients with Fuchs’ syndrome. Ophthalmology 2006; 113: 473–480. 3. Arellanes-Garcia L, Preciado-Delgadillo MDC, Recillas-Gispert C. Fuchs’ heterochromic iridocyclitis: clinical manifestations in dark-eyed Mexican patients. Ocul Immunol Inflamm 2002; 10: 125–131. 4. Norrsell K, SjIˆdell L. Fuchs’ heterochromic uveitis: a longitudinal clinical study. Acta Ophthalmol 2008; 86: 58–64. 5. Mohamed Q, Zamir E. Update on Fuchs’ uveitis syndrome. Curr Opin Ophthalmol 2005; 16: 356–363. 6. Foster CS, Vitale AT. Diagnosis and treatment of uveitis. 2nd ed. New Delhi: Jaypee Brothers; 2013, p. 925–934 chapter 62.
7. Chee SP, Jap A. Presumed Fuchs heterochromic iridocyclitis and Posner-Schlossman syndrome: comparison of cytomegaloviruspositive and negative eyes. Am J Ophthalmol 2008; 146: 883–889. 8. Birnbaum AD, Tessler HH, Schultz KL, et al. Epidemiologic relationship between Fuchs heterochromic iridocyclitis and the United States rubella vaccination program. Am J Ophthalmol 2007; 144: 424–428. 9. Quentin CD, Reiber H. Fuchs’heterochromic cyclitis: rubella virus antibodies and genome in aqueous humor. Am J Ophthalmol 2004; 138: 46–54. 10. De Groot-Mijnes JDF, de Visser L, Rothova A, Schuller M, van Loon AM, Weersink AJL. Rubella virus is associated with Fuchs heterochromic iridocyclitis. Am J Ophthalmol 2006; 141: 212–214. 11. De Visser L, Braakenburg A, Rothova A, de Boer JH. Rubella virus–associated uveitis: clinical manifestations and visual prognosis. Am J Ophthalmol 2008; 146: 292–297. 12. Nizamuddin SHM, Bawazeer AM. Causes of uveitis in a tertiary center in Western Saudi Arabia: a retrospective study. Saudi Med J 2013; 34(4): 179–187. 13. Islam SM, Tabbara KF. Causes of uveitis at The Eye Centre in Saudi Arabia: a retrospective review. Ophthalmic Epidemiol 2002; 9(4): 239–249. 14. Hamade IH, Elkum N, Tabbara KF. Causes of uveitis at a referral center in Saudi Arabia. Ocul Immunol Inflamm 2009; 17(1): 11–16. 15. Al-Mezaine HS, Kangave D, Abu El-Asrar AM. Patterns of uveitis in patients admitted to a University Hospital in Riyadh, Saudi Arabia. Ocul Immunol Inflamm 2010; 18(6): 424–431. 16. Rothova A, La Hey E, Baarsma GS, Breebaart AC. Iris nodules in Fuchs’ heterochromic uveitis. Am J Ophthalmol 1994; 118: 338–342. 17. Jones NP. Fuchs’ heterochromic uveitis: an update. Surv Ophthalmol 1993; 37: 253–272. 18. Al-Mansour YS, Al-Rajhi AA, Al-Dhibi H, Abu El-Asrar AM. Clinical features and prognostic factors in Fuchs’ uveitis. Int Ophthalmol 2010; 30(5): 501–509.