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Photodynamic Therapy for Occult Choroidal Neovascularization With Pigment Epithelium Detachment in Age-Related Macular Degeneration
Ruth Axer-Siegel, MD;
Rita Ehrlich, MD;
Irit Rosenblatt, MD;
Michal Kramer, MD;
Ethan Priel;
Yuval Yassur, MD;
Dov Weinberger, MD
Arch Ophthalmol. 2004;122:453-459.
ABSTRACT
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Objective To study the visual and angiographic outcome of eyes with neovascular age-related macular degeneration associated with pigment epithelium detachment (PED) treated by photodynamic therapy.
Methods Review of the medical charts and the fluorescein and indocyanine green angiograms of all consecutive patients with age-related macular degeneration associated with choroidal neovascularization and serous PED of at least 1 disc diameter, who received photodynamic therapy from January 1, 2000, to August 31, 2002.
Results Thirty patients (34 eyes) met the study criteria. Each underwent 1 to 8 treatments (mean, 4); duration of follow-up was 12 to 36 months (mean, 19 months). Nineteen eyes (56%) lost 3 or more Snellen lines of visual acuity, 7 eyes (21%) lost 1 or 2 lines, 6 eyes (18%) maintained their initial acuity, and 2 eyes (6%) gained 1 or 2 lines. Subretinal hemorrhage occurred in 5 eyes and retinal pigment epithelium tears in 4 eyes. In 4 eyes, visual acuity decreased to counting fingers, hand motions, or light perception.
Conclusions Although 44% of the 34 eyes with age-related macular degeneration and PED lost fewer than 3 Snellen lines in acuity, severe visual loss to counting fingers or less occurred in 4 eyes, 3 of them with choroidal neovascularization inside the PED. Further studies and treatment modalities are required to improve prognosis of neovascular age-related macular degeneration with serous PED.
INTRODUCTION
Photodynamic therapy (PDT) with verteporfin has been shown to be beneficial for the treatment of predominantly classic1-2 and occult with no classic3 subfoveal choroidal neovascularization (CNV) secondary to age-related macular degeneration (AMD). The Macular Photocoagulation Study (MPS)4 recognized 2 forms of occult CNV: fibrovascular pigment epithelium detachment (PED) and leakage of undetermined source. Both forms were included as a single group in the Verteporfin in Photodynamic Therapy study.3 To the best of our knowledge, a separate subgroup analysis of the value of PDT in eyes with neovascular AMD with serous PED associated with CNV has not yet been published.
We herein report the visual and angiographic outcome of a consecutive series of patients with subfoveal occult CNV associated with serous PED of at least 1 disc diameter, who received PDT in a clinical setting.
METHODS
The medical charts and the fluorescein (FA) and indocyanine green (ICGA) angiograms of all consecutive patients with AMD associated with CNV and serous PED who received PDT from January 1, 2000, to August 31, 2002, were reviewed. The study was approved by the Legal Department of the Mor Institute for Medical Data, Bnei Brak, Israel, and all the patients signed an informed consent. The PDT was administered according to the protocol of the Treatment of Age-Related Macular Degeneration With Photodynamic Therapy study,1-2 with follow-up every 3 months for at least 12 months (to September 2003). The need for repeated treatment was determined by the clinician, usually after 3 months. The following data were collected: age and sex; best-corrected Snellen visual acuity (VA) at initial examination and at the end of the follow-up period; number of PDT sessions; and adverse effects of PDT. The FAs and the ICGAs were reviewed by 2 physicians (R.A.-S. and R.E.). The initial diagnosis of CNV associated with serous PED of at least 1 disc diameter was made by FA, and further analysis was performed with ICGA. The CNV was divided into 3 categories by location with respect to the PED, as suggested by Yannuzzi et al5: beneath, CNV located beneath the PED and entirely within its boundaries (Figure 1); contiguous, CNV that interrupted the continuity of the margin of the serous PED (Figure 2); and remote, CNV distinctly separate from the edge of the serous PED (Figure 3).
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Figure 1. A, Fluorescein angiogram showing choroidal neovascularization (CNV) (arrow) beneath pigment epithelium detachment (PED) (arrowheads). B, Leakage from CNV (arrow) and fluorescein pooling of the PED (arrowheads). C, Indocyanine green angiogram (ICGA) demonstrating CNV (arrow) beneath the hypofluorescent PED (arrowheads). D, Late-phase ICGA showing staining of the CNV (arrow) outlined against the hypofluorescent PED (arrowheads).
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Figure 2. Contiguous choroidal neovascularization (CNV). A, Fluorescein angiogram (FA) showing hyperfluorescent choroidal neovascularization (CNV) (arrow) at the margin of pigment epithelium detachment (PED) (arrowheads). B, Late-phase FA showing leaking CNV (arrow) and fluorescein pooling in the PED. C, Indocyanine green angiogram (ICGA) showing the outline of the CNV (arrow) and the hypofluorescent PED (arrowheads). D, Late-phase ICGA demonstrating slight staining of the CNV and the hypofluorescent PED (arrowheads).
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Figure 3. Remote choroidal neovascularization (CNV). A, Fluorescein angiogram (FA) showing hyperfluorescence located below the fovea (arrow) and blocked fluorescence superiorly (arrowheads). B, Late-phase FA demonstrating leakage from the CNV (arrow) and pooling in the pigment epithelium detachment (PED) (arrowheads). C, Indocyanine green angiogram (ICGA) shows a hyperfluorescent spot (arrow) corresponding in location to the CNV shown on the FA. The PED is hypofluorescent (arrowheads). D, Late-phase ICGA shows focal CNV (arrow) and blocked fluorescence corresponding to the PED (arrowheads).
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Correlations were calculated between the initial and final best-corrected Snellen VA, as well as the change in VA after PDT, and the difference in size of the PED, the location of the CNV, and the presence of retinal pigment epithelial (RPE) tear and subretinal hemorrhage.
The  2 test, Fisher exact test, Pearson correlation, and analysis of variance were performed, as appropriate, with the use of SPSS software (version 10, Professional Statistics Release; SPSS Inc, Chicago, Ill).
RESULTS
The cohort included 30 patients (34 eyes) with neovascular AMD associated with PED. There were 18 men and 12 women aged 60 to 90 years (mean, 71.3 years). The number of treatments was 1 to 8 (mean, 4 treatments), and the follow-up period ranged from 12 to 36 months (mean, 19 months).
The best-corrected Snellen VA results are presented in Table 1 and Table 2. An improved VA of 1 or 2 Snellen lines was noted in 2 eyes (6%), no change in VA in 6 eyes (18%), a decrease of 1 or 2 lines in 7 eyes (21%), and a decrease of more than 3 lines in 19 eyes (56%).
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Table 1. Visual Acuity (Snellen) Before and After Treatment
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Table 2. Distribution of Change in Visual Acuity by Location of Choroidal Neovascularization*
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The serous PED composed more than 50% of the lesion in 31 of 34 eyes. Seventeen eyes had CNV beneath the PED, 9 had remote CNV, and 8 had contiguous CNV. The eyes with CNV beneath the PED had the worst VA outcome, with a 65% rate (11/17) of visual loss of 3 lines or more, compared with 44% (4/9) for the group with remote CNV and 50% (4/8) for the group with contiguous CNV. The correlation between the location of the CNV and the change in VA did not reach statistical significance (P = .60, 2 test). Four patients had a final VA of counting fingers, hand motions, or light perception, of whom 3 had CNV beneath the PED and 1 had contiguous CNV. The profound visual loss was due to subretinal hemorrhage in 3 patients (one of whom had an RPE tear as well) and to disciform scar in another patient.
An RPE tear occurred in 4 eyes after 1 or 2 treatments (Table 3). Three of these eyes had CNV beneath the PED, and 1 had contiguous CNV. The VA of these eyes ranged from 20/30 to hand motions. One additional patient had an extrafoveal RPE tear before PDT, and his initial VA of 20/80 remained relatively stable at 20/100 after treatment and throughout 15 months' follow-up.
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Table 3. Visual Acuity of Eyes With Retinal Pigment Epithelial Tear
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Of the remaining 29 eyes, the total lesion size increased in 14 eyes (48%), did not change in 11 (38%), and decreased in 4 (14%) (Table 4). No correlation was found between the change in lesion size and the change in VA (P = .25, 2 test).
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Table 4. Location of Choroidal Neovascularization and Change in Lesion Size (n = 29)*
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Subretinal hemorrhage occurred in 5 eyes, 3 of them with CNV beneath the PED, 1 with remote CNV, and 1 with contiguous CNV. Three of these patients had a final VA of hand motions or light perception, 1 patient had a VA of 20/800, and 1 patient had a VA of 20/200. There was a statistically significant correlation between the presence of subretinal hemorrhage and profound visual loss (P = .03, Fisher exact test).
Four eyes had retinochoroidal anastomoses on ICGA. The VA decreased from 20/60 to 20/150, from 20/25 to 20/50, and from 20/50 to 20/300 in 1 eye each. In the remaining eye, final VA was light perception.
No statistically significant correlation was found between the following variables: initial and final VA; initial VA and subretinal hemorrhage; RPE tear and final VA; final VA and location of CNV; and subretinal hemorrhage and location of CNV (analysis of variance).
COMMENT
The findings of the present study indicate that PDT may be of questionable benefit in eyes with AMD with occult CNV and serous PED. According to the definitions proposed by the MPS,4 there are essentially 2 forms of occult CNV: fibrovascular PED and leakage of undetermined source (without PED). The MPS guidelines (which were used in the Verteporfin in Photodynamic Therapy study3) distinguish between the fibrovascular PED and the typical classic serous detachments of the RPE, which may or may not have detectable CNV on FA. Further modification of the definition of subfoveal neovascular lesions with PED was suggested by Yannuzzi et al,5 who introduced the term vascularized PED to describe the combination of CNV and serous PED of at least 1 disc diameter. This description differs from the MPS terminology, since it includes ICGA findings, whereas the MPS guidelines (which were used in the verteporfin studies1-3) include only FA features. On ICGA, the serous component of the PED is hypofluorescent, whereas the vascularized component is hyperfluorescent, while on FA, both components demonstrate late hyperfluorescence or leakage. Our series included eyes with CNV associated with serous PED of at least 1 disc diameter, and most of the eyes (31/34) included serous PED that was larger than 50% of the lesion (eyes ineligible for verteporfin treatment3). In our study, the diagnosis of exudative AMD was made on the basis of clinical examination, and the presence of occult CNV with serous PED was determined by FA. Pigment epithelium detachment larger than 1 disc diameter associated with CNV was then analyzed by confocal ICGA. On FA, all pigment epithelial elevations, both serous and vascular, stain, whereas on confocal ICGA, the serous PED remains totally dark and the area of hyperfluorescence localizes the neovascularization, thereby segregating the serous and vascularized components. Several reports on the clinicopathological correlation of the hyperfluorescence on ICGA and histopathological proof of CNV support the localization of the CNV at the hyperfluorescent area.6-8
Vascularized PED (serous PED with CNV) accounts for an estimated 26% to 31% of all newly diagnosed cases of exudative AMD.5, 9 Its natural course is poor because of disciform scar formation or RPE tears.9-12 Previous studies on ICGA-guided laser treatment of vascularized PED yielded disappointing visual results.13-15 Slakter et al13 reported anatomic success in only 43% of eyes with vascularized PED compared with 66% in eyes with occult CNV not associated with serous PED. Lim et al14 noted a deterioration in VA in 82% of 20 patients treated by ICGA-guided laser, and Brancato et al15 found a decrease in VA after ICGA-guided laser in 82% of eyes with CNV beneath the PED and in 62.5% of eyes with CNV at the margin of the PED.
The Verteporfin in Photodynamic Therapy study reported that PDT is beneficial in eyes with subfoveal occult CNV with no classic CNV.3 The lesions included in the Verteporfin in Photodynamic Therapy study could contain features that obscured the distinction of classic and occult CNV on FA, namely, blood, hypofluorescence due to sources other than visible blood, and serous PED. Both type 1 (fibrovascular PED) and type 2 (leakage of undetermined source) occult CNV were treated, and no separate analysis of these 2 subgroups was done. Eyes with serous PED occupying more than 50% of the lesion were ineligible for verteporfin. Consequently, there are currently no explicit recommendations for PDT with verteporfin for eyes with subfoveal CNV and serous PED, especially in which the main component of the lesion is serous PED.
To the best of our knowledge, there are as yet no peer-reviewed published studies on series of patients with CNV and serous PED treated with PDT. However, unpublished data and abstracts are available: Pece and Brancato16 reported on 32 PDT-treated eyes of 28 patients with CNV associated with PED followed up for a mean duration of 5.7 months, and Moisseiev et al17 reported on 15 patients with vascularized PED in AMD, in lesions where PED is the predominant component, who received PDT, with a follow-up of 3 to 19 months. Lommatzsch et al18 reported decreased VA of more than 3 lines in 10 (83%) of 12 eyes with vascularized PED treated with PDT, within 3 to 9 months after treatment. Copt and Zografos19 showed that 18 (90%) of 20 eyes with vascularized PED who received PDT lost more than 15 letters of VA from baseline. The results of these series are presented in Table 5. The visual outcome reported in our cohort was decreased VA of 3 or more lines in 56% of the patients, during a follow-up period of 12 to 36 months (mean, 19 months). Our results are similar to those of the smaller series by Moisseiev et al,17 worse than those of the larger series by Pece and Brancato,16 and better than those of the series by Lommatzsch et al18 and Copt and Zografos.19 Although caution must be exercised when different samples are compared, some of the differences may be attributed to the variability in the follow-up periods. It is important to note as well that best-corrected VA from Early Treatment Diabetic Retinopathy Study charts was used in clinical trials for PDT,1-3 whereas best-corrected Snellen VA was used in our retrospective series. Since changes in Snellen lines do not equate with changes in lines on Early Treatment Diabetic Retinopathy Study charts, further caution must be exercised when different series are compared.
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Table 5. Comparison of Visual Acuity Among Series
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The anatomic response to PDT in our patients was disappointing. The lesion size decreased in only 4 eyes, remained stable in 11, and increased in 14 (Table 4).
Tears of RPE occurred in 4 eyes (12%) (Table 3), compared with the rate of 12% in the study by Pece and Brancato,16 33% in the series by Lommatzsch et al,18 and 15% in the study by Copt and Zografos.19 One of our patients with an RPE tear sustained profound visual loss to hand motions because of subretinal hemorrhage, and the other 3 patients had a final VA of 20/30 to 20/200. It is not clear whether these RPE tears are complications of the treatment or represent the natural course of the disease.
Acute RPE tears may occur as a natural complication of CNV associated with PED, or after laser treatment, because of contraction of the underlying CNV or the pressure caused by the sub-RPE fluid on the taut serous PED.20-22 The visual impact of the tear depends on the foveal involvement of the rupture or on the presence of hemorrhages. Several studies reported increased rates of RPE tear after PDT with verteporfin for eyes with CNV associated with PEDs,18-19,23-24 but the mechanism of RPE tear after PDT remains unknown. Immediate optical coherence tomography performed after PDT for subfoveal CNV showed subretinal and intraretinal fluid accumulation caused by leakage from the neovascular complex, which was confirmed by ICGA.25 The fluid accumulation started 120 minutes after PDT and was maintained for up to 5 days. It is therefore possible that this fluid beneath the PED exerts additional tension on the taut RPE, leading to RPE tear.
Subretinal hemorrhage occurred in 5 eyes (one of them with an RPE tear), causing profound visual loss in 4 of them. Three of the eyes had a final VA of hand motions or light perception, one had a VA of 20/800, and one had a VA of 20/200. There was a statistically significant correlation between the presence of subretinal hemorrhage and profound visual loss (P = .03, Fisher exact test).
In conclusion, the visual and anatomic results of our series show that, while 15 (44%) of the 34 eyes lost fewer than 3 lines of Snellen VA after PDT, 4 eyes (12%) sustained profound visual loss, 3 of them because of massive subretinal hemorrhage and 1 because of RPE tear. In addition, 4 eyes (12%) developed RPE tear. No correlation was found between the location of the CNV or the lesion size and the final VA. Although the small sample size precludes definitive recommendations, our study shows a high rate of visual and anatomic complications after PDT in eyes with CNV associated with serous PED.
AUTHOR INFORMATION
Corresponding author and reprints: Ruth Axer-Siegel, MD, Department of Ophthalmology, Rabin Medical Center, Beilinson Campus, Petah Tikva 49 100, Israel (e-mail: seegs{at}netvision.net.il).
Submitted for publication July 23, 2003; final revision received October 31, 2003; accepted December 3, 2003.
This study was presented in part at the meeting of the American Society of Retinal Specialists; August 18, 2003; New York, NY.
From the Department of Ophthalmology, Rabin Medical Center, Beilinson Campus, Petah Tikva, and Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel (Drs Axer-Siegel, Ehrlich, Rosenblatt, Kramer, Yassur, and Weinberger); and Mor Institute for Medical Data, Bnei Brak, Israel (Mr Priel). The authors have no relevant financial interest in this article.
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