INFLAMMATORY DISORDERS

Bromfenac alone or with single intravitreal injectionof bevacizumab or triamcinolone acetonide for treatmentof uveitic macular edema

Alaa E. Radwan & Cheryl A. Arcinue & Paul Yang &

Pichaporn Artornsombudh & Esam M. Abu Al-Fadl &C. Stephen Foster

Received: 18 October 2012 /Revised: 7 February 2013 /Accepted: 4 March 2013 /Published online: 22 March 2013# Springer-Verlag Berlin Heidelberg 2013

AbstractPurpose To evaluate the efficacy of bromfenac drops aloneor with a single intravitreal injection of bevacizumab (IVB)or triamcinolone acetonide (IVTA) in the treatment ofuveitic macular edema (UME).Design Comparative case series.Study Participant Sixty-seven eyes (of 55 patients) withUME that received either bromfenac drops alone (n=34),IVB plus bromfenac (n=21) or IVTA plus bromfenac (n=12).Methods Chart review of patients at the Massachusetts EyeResearch and Surgery Institution (MERSI) was done. Eyesthat received either bromfenac drops alone (Br), IVB plusbromfenac (IVB/Br) or IVTA plus bromfenac (IVTA/Br),with follow-up of up to 3 months, were included.Main Outcome Measure Visual acuity.Results There was no statistically significant effect seen inVA or CMT in the Br group, with 17 of 34 eyes (50 %)

needing re-injection before 3 months of follow-up. Meanchange in CMT at 4 weeks for the Br group was 5.06 µm.Compared to baseline, both the IVTA/Br and IVB/Br groupsshowed significant decrease in CMTand improvement in VA at1 and 3 months follow-up. There was also a continuous de-crease in CMT up to 3 months of follow-up with the IVTA/Brgroup, which was found to be significant in comparison withthe IVB/Br group; this trend was not seen in the IVB/Br groupat 3 months. The greatest mean change in CMTat 1 month wasseen in the IVTA/Br group (154.33 ±178.22 µm), and this wasstatistically significant in comparison with the other groups(p=<0.0001). However, in terms of mean change in VA, therewas no change in the Br group (0.01±0.11 VA logMAR), andonly 0.12±0.19 and 0.15±0.20 in the IVB/Br and IVTA/Brgroups, respectively.Conclusion IVB and IVTA are both effective in improvingVA and decreasing CMT up to 3 months. Bromfenac isineffective alone for UME treatment, but may have a syn-ergistic effect with IVTA in reducing CMT up to 3 monthsof follow-up.

Keywords Macular edema . Bromfenac . Bevacizumab .

Triamcinolone acetonide

Introduction

Macular edema secondary to uveitis is a major complication,occurring in up to 48 % of uveitis cases [1], and associatedmore commonly with intermediate, posterior, and panuveitis[2]. Cystoid macular edema (CME) is the main cause of visualloss in patients with intraocular inflammation [3].

The pathogenesis of CME is not clear and may resultfrom dysfunction of and/or injury to either the inner or the

A. E. Radwan : C. A. Arcinue : P. Yang : P. Artornsombudh :C. S. Foster (*)Massachusetts Eye Research and Surgery Institution (MERSI),8th Floor, 5 Cambridge Center,Cambridge, MA 02142, USAe-mail: fosters@uveitis.org

A. E. Radwan : C. A. Arcinue : P. Yang : P. Artornsombudh :C. S. FosterOcular Immunology and Uveitis Foundation,Cambridge, MA, USA

C. S. FosterDepartment of Ophthalmology, Harvard Medical School,Boston, MA, USA

E. M. Abu Al-FadlDepartment of Rheumatology and Rehabilitation,Sohag Faculty of Medicine, Sohag University, Sohag, Egypt

Graefes Arch Clin Exp Ophthalmol (2013) 251:1801–1806DOI 10.1007/s00417-013-2309-4

outer blood-eye retinal barrier. However, it is clear thatuntreated uveitic CME tends to cause progressive injury tothe macula. CME can be classified as angiographic (leakagedetected on fluorescein angiography), clinical (biomicroscopicor angiographic leakage in combination with visual impair-ment), and most recently, in terms of retinal thickening asmeasured by optical coherence tomography (OCT). Actually,OCT is as good as fluorescein angiography for detectinguveitic CME and superior in demonstrating the distributionof fluid within the retina [4].

Medical treatment of uveitic macular edema includestopical and systemic nonsteroidal anti-inflammatory drugs(NSAIDs), corticosteroids (topical, systemic, transseptal, orintravitreal), and systemic carbonic anhydrase inhibitors.Topical NSAIDs have been efficacious in the prophylaxisand/or treatment of aphakic CME [5, 6]. Treatment with thenew-generation NSAID, nepafenac 0.1 %, in acutepseudophakic CME strongly suggests that nepafenac0.1 % is a promising drug for treatment of CME [7].Bromfenac is structurally identical to amfenac (nepafenac)with the exception of bromine at the C4 position, whichincreases penetration into ocular tissue, extends duration ofanti-inflammatory activity, and enhances inhibitory effect onCOX-2 [8].

Intravitreal injection of bevacizumab (IVB) as well asintravitreal triamcinolone acetonide (IVTA) are well toleratedand is associated with short-term improvement in visualacuity (VA) and decreased OCT retinal thickness in aconsiderable proportion of patients with uveitic CME resis-tant to conventional therapy [9, 10]. Tranos and associates[11] found in a long-term follow-up study of inflammatorymacular edema up to 49 months, that visual acuity 1 monthafter treatment is usually indicative of the final functionaloutcome.

The purpose of this study is to assess the efficacy ofbromfenac sodium ophthalmic solution alone or afterintravitreal injection of bevacizumab or triamcinolone

acetonide in the treatment of uveitic macular edema by mea-surement of visual acuity (VA) and assessment of centralmacular thickness (CMT) using optical coherence tomography(OCT).

Materials and methods

Study design

This is a retrospective comparative case series. The databaseof the Massachusetts Eye Research and Surgery Institution(MERSI) from 2005 to 2011 was thoroughly searched andall patients with uveitic CME who received bromfenac eyedrops alone (Br) or in combination with either intravitrealbevacizumab (IVB/Br) or intravitreal triamcinoloneacetonide (IVTA/Br) were included in the study. The uveitisat the time of treatment had to be in remission. Patients whohad intraocular surgery within 3 months of the onset ofmacular edema were excluded from this study. The follow-up period was up to 3 months for all the patients included inthe study. All patient information was kept strictly confiden-tial. Written informed consent was obtained for each patientprior to the procedures. Institutional Review Board (IRB)approval was acquired for this review and analysis of patientdata.

Treatment protocol

Intravitreal injection of triamcinolone acetonide (IVTA) orbevacizumab (IVB) was carried out under aseptic condi-tions. Triesence (Alcon Laboratories Inc.) 40 mg/mL wasused with a dose of 4 mg/0.1 mL and bevacizumab(Genentech) 25 mg/mL dose was given. A topical anestheticand 5 % povidone iodine solution was instilled on the con-junctival sac prior to injection. The intravitreal injection wasperformed using a 27-gauge needle in the superotemporal

Table 1 Baseline demographic characteristics

Baseline Characteristics Overall(n=67)

Bromfenac(n=34)

Bevacizumab +Bromfenac (n=21)

IVTA + Bromfenac(n=12)

p-value

No. % No. % No. % No. %

Age (mean ± SD) 54.8±14.1 56.1±13.9 54.6±13.7 52.1±16.0 0.73a

Sex 0.009b

Male 15 27.3 4 15.4 4 22.2 7 63.6

Female 40 72.7 22 84.6 14 77.8 4 36.4

Baseline visual acuity (in logMAR) 0.46±0.32 0.39±0.28 0.55±0.24 0.52±0.50 0.153a

Baseline central macular thickness (in um) 399.22±139.16 353.97±96.91 459.14±154.86 422.58±175.03 0.018a

a ANOVA testb Chi-square test

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quadrant, 3.5 (in aphakic or pseudophakic eyes) to 4.0 mm(phakic eyes) posterior to the limbus. Bromfenac sodium eyedrops were used twice a day.

Study outcomes

The primary efficacy outcome of this study was visualacuity (VA) before and after the use of bromfenac eye dropsalone or in combination with intravitreal bevacizumab ortriamcinolone acetonide. The secondary efficacy outcomewas the mean central macular thickness (CMT) on OCTbefore and after the use of bromfenac eye drops alone orin combination with intravitreal bevacizumab or triamcino-lone acetonide.

Statistical analysis

Data were analyzed using IBM SPSS statistical softwarepackage version 19. Baseline characteristics (age, sex, visu-al acuity and central macular thickness) were compared toassess comparability of the two groups. Chi-square test wasused to compare sex, and ANOVA test was used to comparethe mean age. The t test was used to compare the mean VAand CMT between two groups, while ANOVA test was usedto compare the three groups. ANOVA test was also used tocompare the mean change in VA and CMT at the 1-monthfollow-up period. Paired sample t-test was used for

comparison of VA and CMT across time in each group.Post-hoc test (Bonferroni) was also carried out to assess thesignificance of differences found between groups. A p-valueof 0.05 or less (level of significance) was consideredstatistically significant.

Results

Baseline demographic characteristics

A total of 67 eyes (of 55 patients) that received bromfenacsodium (Br) eye drops alone (n=34 eyes of 26 patients),intravitreal bevacizumab with bromfenac sodium (IVB/Br)(n=21 eyes of 18 patients), or intravitreal triamcinoloneacetonide with bromfenac sodium (IVTA/Br) (n=12 eyesof 11 patients) were included in this study. Baseline de-mographics are shown in Table 1. There were no significantdifferences in baseline demographic characteristics in termsof age and baseline visual acuity. There were more femalesthan males in the Br and IVB/Br groups, and the baselinecentral macular thickness was statistically higher in theIVB/Br group (p=0.018). Uveitis diagnosis is shown inTable 2. The majority of patients had idiopathic panuveitisin all the three groups.

Visual acuity

Comparison of VA between the three groups and across timeis shown in Table 3. Baseline VA in the IVB/Br group wasstatistically lower compared with the Br group (p=0.031).At 1 month and 3 months follow-up, there were no statisti-cally significant differences between the 3 groups. In the Brgroup, there was no statistically significant difference be-tween baseline VA and VA at 1 and 3 months. In the IVB/Brgroup, VA at 1 month and 3 months were statistically bettercompared with baseline VA (p=0.010 and p=0.001, respec-tively). However, there was no statistically significant dif-ference between VA at 1 month and 3 months (p=0.149). Inthe IVTA/Br group, the VA at 1 month and 3 months wasalso statistically better compared with baseline VA (p=0.031 and p=0.017, respectively). Comparison of VA at1 month to VA at 3 months was also not significantlydifferent (p=0.250).

Table 2 Uveitis diagnosis (per patient)

Diagnosis Bromfenac Bevacizumab +Bromfenac

IVTA +Bromfenac

Idiopathic uveitis

Anterior 5 4 2

Intermediate 6 2 3

Posterior 3 1 0

Panuveitis 6 9 4

Sarcoid-associateduveitis

4 2 2

Birdshotretinochoroidopathy

1 0 0

Vogt-Koyonagi-Harada syndrome

1 0 0

Total 26 18 11

Table 3 Comparison of visualacuity between groups andacross time (Mean ± SD)

aANOVA testbPaired sample T test

VisualAcuity

Overall(n=67)

Bromfenac(n=34)

Bevacizumab +Bromfenac (n=21)

IVTA + Bromfenac(n=12)

p-value

Baseline 0.46±0.32 0.39±0.28 0.55±0.24 0.52±0.50 0.153a

1 month 0.39±0.34 0.37±0.29 0.43±0.29 0.37±0.53 0.829a

3 months 0.33±0.35 0.31±0.27 0.35±0.23 0.33±0.55 0.928a

0.911b 0.001b 0.017b

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Central macular thickness

Comparison of CMT between the three groups and acrosstime is shown in Table 4. Baseline CMT in the IVB/Brgroup was statistically higher compared with the Br group(p=0.018). Post—hoc analysis reveals a significant differ-ence in baseline CMT between the Br and IVB/Br groupsonly (p=0.017); no significant differences were found be-tween the Br and IVTA/Br (p=0.385) and between theIVB/Br and IVTA/Br (p=1.00) groups. At 1-monthfollow-up, the IVTA/Br group had significantly thinnerCMT compared with the Br and IVB/Br groups (p=0.004and p=0.041, respectively). However, on post-hoc analysis,there were no significant differences found between allthe three groups. There were no statistically significantdifferences in CMT between the 3 groups at 3 monthsfollow-up.

In the Br group, there was no statistically significantdifference between baseline CMT and CMT at 1 and3 months (p=0.482 and p=0.145, respectively). In theIVB/Br group, CMT at 1 month and 3 months were statis-tically thinner compared with baseline CMT (p=0.001 andp=0.002, respectively). However, there was no statisticallysignificant difference between CMT at 1 month and3 months (p=0.398). In the IVTA/Br group, the CMT at1 month and 3 months was also statistically better compared

with baseline CMT (p=0.012 and p=0.009, respectively). Inthis group, comparison of VA at 1 month to VA at 3 monthswas significantly different (p=0.015).

Mean change in CMT and VA at 1-month follow-up

Mean change in CMTandVA at the 1-month follow-up periodis shown in Table 5. The greatest mean change in CMT at1month was seen in the IVTA/Br group (154.33 ±178.22 um),and this was statistically significant in comparison with theother groups (p<0.0001). Post-hoc analysis of the meanchange in CMT at 1-month follow-up reveals a statisticallysignificant difference between the Br and IVB/Br groups (p=0.003) and between the Br and IVTA/Br groups (p<0.0001).However, in terms of mean change in VA, there was nosignificant change in the Br group (0.01±0.11 VA logMAR),and only 0.12±0.19 and 0.15±0.20 in the IVB/Br andIVTA/Br groups, respectively. This change in logMAR isequivalent to only 1 line improvement in Snellen VA. Post-hoc analysis of the mean change in VA at 1-month follow-upshows a nearly significant difference between the Br andIVB/Br (p=0.058) and between the Br and IVTA/Br (p=0.053) groups. Despite the greater mean change in CMT seenin the IVTA/Br group compared with the IVB/Br group (p=0.535), the mean change in VA between these 2 groups wasalmost the same (p=1.00).

Table 4 Comparison of central macular thickness between groups and across time

Central MacularThickness (CMT)

Overall (n=67) Bromfenac(n=34)

Bevacizumab +Bromfenac (n=21)

IVTA + Bromfenac(n=12)

p-value Post-hoc testc p-value

Br vs.IVB/Br

Br vs.IVTA/Br

IVB/Br vs.IVTA/Br

Baseline 399.22±139.16 353.97±96.91 459.14±154.86 422.58±175.03 0.018a 0.017 0.385 1.00

1 month 336.69±105.13 348.91±89.21 356.00±137.43 268.25±42.58 0.041a 1.00 0.063 0.060

3 month 286.42±67.83 301.82±63.19 288.29±81.12 259.73±46.19 0.279a 1.00 0.341 0.838

0.145b 0.002b 0.009b

a ANOVA testb Paired sample T testc Post-hoc test (Bonferroni)

Table 5 Comparison of mean change in central macular thickness and visual acuity at 1-month follow-up between groups

Mean Change at1-Month Follow-Up

Bromfenac(n=34)

Bevacizumab +Bromfenac (n=21)

IVTA + Bromfenac(n=12)

p-value Post-hoc testb p-value

Br vs.IVB/Br

Br vs.IVTA/Br

IVB/Br vs.IVTA/Br

CMT (in um) 5.06±41.51 103.14±119.43 154.33±178.22 <0.0001a 0.003 <0.0001 0.535

VA (in logMAR) 0.01±0.11 0.12±0.19 0.15±0.20 0.016a 0.058 0.053 1.00

a ANOVA testb Post-hoc test (Bonferroni)

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Discussion

Bromfenac is an attractive NSAID agent, which can achievetherapeutic levels in the retina after topical application ontothe cornea, and has minimal complications or side effects [12].However, no studies have been published on the efficacy ofbromfenac ophthalmic solution alone or with intravitrealbevacizumab or triamcinolone acetonide injection to treatCME in patients who have had uveitis.

Prevention ofmacular edema and ocular inflammationwithbromfenac after cataract surgery in non–insulin-dependentdiabetic patients was reported [13, 14]. In the current study,we did not find any significant effects on VA and CMT withbromfenac ophthalmic solution alone in the treatment of CMEin uveitic patients, with 50 % of the study eyes needingadditional intervention after 4 weeks due to deterioration ofVA due to worsening of macular edema.

Kok et al [15] reported that the best visual outcome afterIVTA injection for uveitic macular edema occurred at a meanof 4 weeks. Of his patients, 51% had significant response withat least two-fold improvement in visual acuity. However, onethird of them experienced a decrease in VAwithin 4.2 monthsafter treatment, with worsening CME confirmed by OCTand/or FA. Our results in the IVTA/Br group showed similarresults in that the best visual outcome in terms of VA improve-ment and greatest CMT decrease was at 4 weeks. Moreover,there was continuous decrease in CMT for 12 weeks withstable or improved visual acuity except for 2 eyes (16.67 %),which showed a decrease of visual acuity of one line (0.1logMAR) over 12 weeks. In our study, all eyes that had stableor improved VA also showed stable or continuous decrease ofCMT. In another interesting study of quiescent uveitic patients(24 eyes) with CME treated with IVTA, 19 eyes needed to bereinjected by 12 weeks [16].

Soheilian and associates [17] compared intravitrealbevacizumab (IVB) and intravitreal triamcinolone acetonide(IVTA) in treatment of refractory uveitic macular edema,and found that there was no significant difference in VA andCMT between the two groups at 36 weeks. Additionally,Bae et al [18] demonstrated that IVTA was better than IVBor posterior subtenon injection of TA, however the differ-ence did not reach statistical significance. Lasave et al. [19]found the same results of superiority of IVTA compared toIVB treatment in 36 eyes which had refractory uveitic CMEthat had been unresolved by previous systemic, topical, orperiocular treatment. In our study, eyes in the IVB/Br grouphad the worst VA and CMT at baseline. But despite this fact,at 1-month follow-up, the IVTA/Br group still had greaterdecrease in CMT compared with the IVB/Br group, and thiswas found to be statistically significant. We hypothesize thatthe reason for this is that IVTA/Br is more effective inreducing CMT in patients with uveitic CME because of itsanti-inflammatory effects and its beneficial role in

stabilizing the blood-retinal barrier. Additionally, bromfenacmay have an additive effect with IVTA in the treatment ofeyes with uveitic CME as it is also an anti-inflammatoryagent. However, despite the fact that there was a greatermean change in CMT at 1-month follow-up in the IVTA/Brgroup compared with the IVB/Br group, the mean change inVA at this period was almost the same for the these twogroups, showing that a decrease in CMT does not alwaysequate to a corresponding improvement in VA.

Intravitreal injection of bevacizumab (IVB) was reportedto be effective in the management of pseudophakic oruveitic CME in previous studies [20–22]. Our results vali-date previous findings that IVB can significantly reduceCMT and improve VA up to 3 months of follow-up. How-ever, compared to the IVTA/Br group, the IVB/Br groupwas not significantly better.

This study has several limitations. First, since this is aretrospective study, the inherent potential problems associ-ated with this type of analysis are present. Additionally, thesample size is small for the three groups, especially theIVTA/Br group, limiting the power of the study to detect atrue difference between the three groups if present. Furtherprospective randomized controlled trials need to be under-taken to truly detect if there is any difference between thesetreatments. Specifically, the combination of IVTA withbromfenac needs to be compared with the use of IVTA aloneto truly elucidate the effect of this combination.

In conclusion, bromfenac is ineffective alone, and boththe IVTA/Br and IVB/Br treatments were effective for de-creasing macular thickness and recovering visual losscaused by uveitic macular edema. The greatest CME de-crease at 1 month was seen with the IVTA/Br group, whichdid not correspond to a greater improvement in VA. Therewas also a continuous decrease in CMT up to 3 months offollow-up with the IVTA/Br group, which was found to besignificant; this trend was not seen in the IVB/Br group at3 months. Based on this, bromfenac may have a synergisticeffect with IVTA in decreasing CMT up to 3 months becauseboth of them are anti-inflammatory. However, further com-parative studies need to be done to prove this hypothesis.

Financial support None

Conflict of interest No conflicting relationship exists for any author

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