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Prospective Clinical Trial Evaluating the

Efficacy of Photodynamic Therapy for


Symptomatic Circumscribed Choroidal
Hemangioma
Anna Boixadera, MD,1 José García Arumí, MD,1,2 Vicente Martínez-Castillo, MD,1 Jose Luis Encinas, MD,3
Javier Elizalde, MD,4 Gonzalo Blanco-Mateos, MD,5 Jose Caminal, MD,6 Carmela Capeans, MD,7
Félix Armada, MD,8 Amaparo Navea, MD,9 Jose Luis Olea, MD10

Purpose: To evaluate photodynamic therapy (PDT) for symptomatic circumscribed choroidal hemangioma (CCH).
Design: Prospective, multicenter, nonrandomized clinical trial.
Participants: Thirty-one eyes of 31 patients with posterior pole CCH and symptoms caused by exudation
into the macular area.
Intervention: Photodynamic therapy was applied by Zeiss laser. Intravenous verteporfin at 6 mg/m2 body
surface was administered before treatment, and light emitted at 689 nm for photosensitization. The treatment
spot diameter was calculated on early-phase frames of pretreatment indocyanine green angiography. Fifteen
minutes after starting the verteporfin infusion, the laser beam was applied to the retina at radiant exposure 50
J/cm2 and exposure time 83 seconds. One to 4 treatments were applied at 12-week intervals over 1 year.
Standardized evaluation was performed before and at 4-week intervals after each treatment, and at 3, 6, 9, and
12 months. All patients were followed for ⱖ12 months.
Main Outcome Measures: The primary outcome measure was the absence of exudative retinal detachment at the
12-month follow-up visit on ophthalmoscopy, fluorescein angiography, and optical coherence tomography. Secondary
measures were the visual acuity outcome, with best-corrected visual acuity determined by the Early Treatment for Diabetic
Retinopathy Study chart, tumor thickness decrease on B-scan ultrasonography, and adverse events.
Results: Among the total, 82.8% of patients required 1, 13.8% 2, and 3.4% 3 PDTs to eliminate exudative
retinal detachment. Visual acuity increased from a mean of 20/60 to 20/35 (P⬍0.001). Sixty-nine percent of
patients demonstrated visual recovery (P⬍0.001). Cystoid macular edema regressed in all cases and exudative
macular detachment disappeared in all but 2 cases. The CCH thickness decreased in all cases from a mean of
3.0 to 1.7 mm, with the most intense effect seen after 4 weeks of treatment (P⬍0.001). Visual fields showed
resolution of central scotomas. There were no severe adverse events.
Conclusions: Combining PDT with the standard age-related macular degeneration protocol is an effective
treatment for CCH in terms of resolution of exudative subretinal fluid and recovery of VA.
Financial Disclosure(s): The authors have no proprietary or commercial interest in any materials discussed
in this article. Ophthalmology 2009;116:100 –105 © 2009 by the American Academy of Ophthalmology.

Choroidal hemangioma is a benign, relatively rare hamar- exudative retinal detachment, hyperopic shift, degeneration
tomatous tumor that occurs in 2 forms: more frequently as of the retina overlying a subfoveal tumor, or rarely, forma-
a circumscribed isolated lesion and less commonly as a tion of a neovascular choroidal membrane.2
diffuse form associated with Sturge-Weber syndrome.1 Cir- Xenon arc, argon laser photocoagulation, and transpupil-
cumscribed choroidal hemangioma (CCH) presents as a lary thermotherapy have been used to treat CCH with lo-
discrete, smooth, round or slightly oval, orange-red mass calized retinal detachment. All these techniques have lim-
posterior to the equator, mainly in the macular and peripap- ited efficacy, recurrences are not uncommon, and the scar
illary region,1 with rather indistinct margins. Anatomic and affects the foveola in central lesions.3– 8
functional symptoms vary considerably and range from an Photodynamic therapy (PDT) is a potent vasocclusive
asymptomatic lesion found incidentally to cases of severe modality that selectively maintains neuroretinal structures.9
vision loss.1 The associated chronic exudation strongly Highly vascularized choroidal tumors experimentally im-
compromises visual acuity (VA) in some patients. Treat- planted into the suprachoroidal space have responded with
ment is indicated if VA decreases because of secondary complete regression.10 This evidence, together with the

100 © 2009 by the American Academy of Ophthalmology ISSN 0161-6420/09/$–see front matter
Published by Elsevier Inc. doi:10.1016/j.ophtha.2008.08.029
Boixadera et al 䡠 PDT for Symptomatic Circumscribed Choroidal Hemangioma

effectiveness of PDT for reducing leakage from choroidal and 6th months. Patients who had not been retreated at that time
neovascularization,11 support the benefit of PDT use in were followed up at 6 months. The same follow-up regimen was
patients with CCH. used in all patients for the 6- to 12-month visits. Treatment was
Pilot studies using different treatment protocols have stopped when exudation resolved completely. Persistence of a
residual tumor mass was not an indication for retreatment. Table 1
shown promising results with PDT.12–28 The purpose of this shows the schedule of follow-up visits.
study is to evaluate PDT with the standard age-related Adverse events and complications were immediately recorded
macular degeneration (AMD) PDT protocol on a multi- by both the study organizer and the contract research organization.
center clinical trial basis, using fluorescein angiography and The percentages of treatment responses with 95% confidence
optical coherence tomography (OCT) to monitor the pres- intervals were calculated using SPSS software (version 13.0).
ence of subretinal fluid. Visual acuity changes, tumor height decrease, and relapses of
exudative retinal detachment were assessed with the Cochrane
Q-test. The McNemar test was used to compare the results of the
Methods various examinations performed at the follow-up visits. The
changes in foveal thickness on OCT and changes in VA and tumor
This is a prospective, nonrandomized, multicenter clinical trial height on B-scan ultrasonography between the baseline visit and
carried out in 10 centers in Spain. The trial started on January 12, the 12-month follow-up visit were analyzed with the Wilcoxon
2005, and enrollment ended on October 25, 2005. The study test.
protocol was approved by the Ethics Committees of all participat-
ing hospitals.
One eye from each of 31 patients was included in this clinical
trial. The diagnosis of CCH was based on findings obtained by Results
ophthalmoscopy, indocyanine green (ICG) and fluorescein angiog-
raphy, and B-scan ultrasonography. The study included 17 men and 12 women with a mean age of
All patients completed a follow-up of 12 months. Thirty-one 48.6⫾14.6. Presenting symptoms included blurred vision in all pa-
CCH with subfoveal subretinal fluid on OCT (OCT 3; Humphrey tients with a mean time from onset of 24.6 months. Metamorphopsia
Instruments, Dublin, CA) were treated with PDT 1– 4 times during and scotoma were present in 58.6% and 48.3%, respectively.
1 year of follow-up. Seven angiomas (24.1%) had been treated previously: 5 with
Inclusion criteria were patients ⱖ18 years of age with CCH laser (2 of these also with transpupillary thermotherapy) and 2 with
showing a maximum height of 5 mm and maximum diameter of 12 transpupillary thermotherapy. The CCH was located at the macula
mm, and exudative retinal detachment affecting the fovea. Patients in 68.9% (subfoveal 10.3%, juxtafoveal 24.1%, extrafoveal
with treated CCH were eligible for inclusion, but the last treatment 34.5%), in the peripapillary area in 37.9%, and in a temporal
had to be ⱖ6 months before enrollment, and there could be no location in 17.2%. Visual field defects were present in all patients
cataract or cataract surgery within the last 2 months. Patients were and included central defects without fixation point involvement in
excluded if they were taking photosensitive drugs, had cataracts or 48.1% and central defects with affected fixation point in 51.9%.
underwent cataract surgery within the last 2 months, porphyria, Mean maximum diameter of the CCH was 6.6⫾1.7 mm, based on
significant liver disease, active hepatitis, gravidity, ocular disease early phase ICG angiography frames. Twenty-four patients (82.8%)
that could affect VA, noncontrolled high blood pressure, or New required 1 PDT, 4 (13.8%) required 2 PDTs, and 1 patient (3.4%)
York Heart Association class III–IV heart failure. Fertile woman required 3 PDTs. Only 2 patients (6.9%) relapsed; that is, subreti-
required a pregnancy test before enrollment and all patients signed nal fluid that had disappeared at the previous follow-up visit had
a written informed consent form for participation. Two patients reappeared at the next visit.
who did not meet all inclusion criteria were excluded from the The treatment was well-tolerated in all patients and there were
statistical analyses. no side effects. At the 12-month follow-up visit, 93% of patients
Best-corrected VA was determined using the Early Treatment showed no exudation (Figs 1 and 2). Mean pretreatment foveal
for Diabetic Retinopathy Study chart. thickness on OCT was 332⫾157 ␮m. Mean pretreatment subreti-
Ophthalmoscopy, ICG and fluorescein angiography, 120-point nal fluid height was 262⫾279 ␮m, and 48% of patients had
Humphrey visual field testing, 50° fundus photography, OCT pretreatment cystoid macular edema. Mean posttreatment foveal
study, and B-scan ultrasonography were performed in all patients thickness was 253⫾330 ␮m, with a significant difference as com-
within 1 week before the first treatment and at follow-up visits, pared with the pretreatment value (P ⫽ 0.0018). Cystoid macular
with the exception of ICG angiography (only at baseline) and edema regressed in all cases. Visual fields showed clearing of
visual field testing (baseline and 6-month follow-up). The standard central scotomas in all patients.
AMD PDT protocol was applied by Zeiss laser (Visulas 6905, Carl Visual acuity increased from a mean of 20/60 to a mean of
Zeiss-Meditec AG, Jena, Germany) at baseline and, if required, at 20/35 (P⬍0.001). Recovery of VA was documented in 69% of
the 3-, 6-, and 9- month follow-up visits. Photodynamic therapy patients (20/29), 27.5% remained stable (8/29), and 1 patient
consisted of verteporfin administration at 6 mg/m2 body surface showed a marginal VA decrease. Patients in whom VA was
area (Visudyne; Novartis Ophthalmics AG, Basel, Switzerland), ⱕ20/200 before PDT showed slight, if any, improvement during
and a light dose of 50 J/cm2 at 692 nm. If the diameter of the tumor therapy. Marked VA recovery was also observed in patients with
(based on ICG early phase frame measurements) exceeded the a longstanding subfoveal lesion.
maximum spot size, several spots were applied to cover the CCH Circumscribed choroidal hemangioma thickness decreased in
area, while attempting to avoid overlapping. If the CCH was close all cases from a mean pretreatment thickness on B-scan ultra-
to the optic disc, a margin of 200 microns was left. Follow-up sonography of 3⫾1 mm to a mean of 1.7⫾0.9 mm (P⬍0.001).
visits were carried out at 1, 2, and 3 months after the first treat- Patient characteristics are shown in Table 2 (available online at
ment. Patients were retreated when subretinal fluid (⬎50 microns) http://aaojournal.org).
was documented on fluorescein angiography or OCT within 3 No damage to the retinal vessels was observed, although the
months after the last treatment. If patients had been retreated in the choroidal vessels could not be directly assessed, because posttreat-
3rd month, further follow-up visits were scheduled for the 4th, 5th, ment ICG angiography was not performed.

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Ophthalmology Volume 116, Number 1, January 2009

Table 1. Schedule of Follow-up Visits

V1
V0 First
Preinclusion Treatment V2 V3 V4 V5 V6 V7 V8 V9 V10
Visit (<1 week 1 mo ⴞ 2 mos ⴞ 3 mos ⴞ 4 mos ⴞ 6 mos ⴞ 7 mos ⴞ 9 mos ⴞ 10 mos ⴞ 12 mos ⴞ
Test (screening) from V0) 1 wk 1 wk 15 d 15 d (IR) 15 d 15 d (IR) 15 D 15 D (IR) 15 d
Selection criteria X
Pregnancy test X X X X X
Blood test X
Diagnosis X
Premature end of trial
Reason for patient loss X X X X X X X X X X
Biodemographic data
Date of birth X
Gender X
Height X X X X
Weight X X X X
Blood pressure X X X X X
Heart rate X
Personal history
Smoking X
High blood pressure X
Diseases and concomitant X X X X X X X X X X
treatment
Ophthalmic history
Previous treatment for X
CCH
Eye with CCH X X X X X X X X X X
Symptoms X X X X X X X X X X
Visual acuity (ETDRS) X X X X X X X X X X
Subjective refraction X X X X X X X X X X
Ancillary ophthalmic tests
Visual field X X
Funduscopy X X X X X X X X X X
Retinography 50° X X X X X X X X X X
Fluorescein angiography X X X X X X X X X X
Indocyanine green X
angiography
B-mode ultrasonography X X X X X X X
Optical coherence X X X X X X X X X X
tomography
Treatment
Treatment administered X X X X
Side effects X X X X X X X X X X

CCH ⫽ circumscribed choroidal hemangioma; ETDRS ⫽ Early Treatment for Diabetic Retinopathy Study visual acuity chart; IR ⫽ if the patient has
been retreated; M ⫽ month.

Discussion Earlier treatments used for symptomatic CCH have been


effective, but recurrences are common and there is a risk of
This study presents the only clinical trial and the largest prospec- vision loss in patients with foveolar involvement.3– 8 Pho-
tive study reported to date of CCH treated with PDT. Regarding tocoagulation is one of these treatment options. This tech-
the natural history of this condition, the most complete clinical nique only reaches the surface of the tumor and is unable to
study of CCH is contained in the published reports of a group of eliminate it. Recurrence of leakage is common and leads to
patients from the Wills Eye Hospital. The latest report29 includes progressive vision loss.5,6 External radiation delivered by
200 patients, among whom 81% had exudative retinal detachment x-rays or proton beam, plus brachytherapy, have been
at the time of presentation. The clinical manifestations and factors shown to induce complete reattachment and even complete
predictive of final visual outcome are described. The authors tumor regression, but brachytherapy requires 2 surgical
concluded that, in the long term, approximately 50% of the pa- procedures, and as occurs with all types of irradiation, there
tients will have a VA outcome of ⱕ20/200, particularly owing to is a risk of local and systemic complications.6 Transpupil-
chronic macular edema. Augsburger et al3 reported the long-term lary thermotherapy is another therapeutic option for CCH
visual prognosis in these patients; 75% had VA values ⬍20/50 that causes secondary changes in the photoreceptor and
despite treatment. retinal pigment epithelium (RPE) layers.7,8 Thermotherapy

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Boixadera et al 䡠 PDT for Symptomatic Circumscribed Choroidal Hemangioma

Figure 1. Ophthalmoscopic appearance of choroidal hemangioma before and after photodynamic therapy (PDT) in Patient 15. A, A vascular tumor
extending through the superior temporal vascular arcade is seen at presentation; visual acuity (VA) was 20/40. B, Pretreatment optical coherence
tomography (OCT) shows subretinal fluid over the tumor and subfoveal exudative detachment. C, Twelve weeks after the first PDT treatment, the
hemangioma has flattened slightly and shows no exudation VA was 20/20 at this follow-up visit. D, Posttreatment OCTs show no subretinal fluid over
the tumor and foveal restoration with absence of subfoveal fluid.

is a good option for extramacular CCH, but it should not be ranges from 50 to 100 J/cm2 in the reported series. Porrini
used in subfoveal cases as the first choice. et al19 treated lesions ⬍2 mm in height with 75 J/cm2 and
Photodynamic therapy allows selective photochemical in- an exposure time of 125 seconds. Lesions ⬎2 mm in height
jury only to the vascular endothelial cells, while preserving received 100 J/cm2 with an exposure time of 186 seconds.
other retinal structures. The mechanism of action of PDT in Verbraak et al25 described similar results with radiant ex-
CCH may be similar to that occurring in choroidal neovascu- posure doses of 50 and 100 J/cm2.
larization, but there are no histopathologic studies to confirm The initial treatment protocol used also differs. Some
this.9,11 The use of PDT for symptomatic CCH is based on authors apply a single spot covering the entire lesion15,19;
experimental studies in animals with choroidal tumors. These others use a single spot only large enough to cover “the
efforts have shown that a photosensitizer administered intra- most prominent part” of the tumor,25 and still others apply
venously and exposure to a laser at a wavelength of 692 nm ⱖ1 overlapping spots12,27 or nonoverlapping spots.16,18,23
produces tumor necrosis by photothrombosis of endothelial The number of treatment sessions in the reported series
membranes.10 Photodynamic therapy is a safe, rapid, widely ranges from 1 to 5, at intervals of 6 –12 weeks.
available outpatient procedure. As compared with the other In addition to eliminating the serous retinal detachment in
treatment options, it is more suitable for use in subfoveal CCH. almost all patients, PDT reduces the tumor height either markedly
In contrast, brachytherapy is a surgical procedure and proton or completely. Nonetheless, there is no reported evidence that the
beam therapy is less commonly available.5,6 objective of treatment should be tumor regression. Based on their
Several clinical series of patients with CCH treated by PDT experience, Porrini et al19 believe that the treatment goal should be
with different protocols have been described, with authors elimination of subretinal fluid and occlusion of the vascular net-
reporting an overall favorable outcome.12–28 Thus, the cur- work with complete regression of the tumor to prevent recurrence.
rently available therapy that seems to produce the best clinical In contrast, Jurklies et al,18 who have described the largest group
results for exudative retinal detachment in CCH is PDT. treated to date (19 patients), contend that retreatment is only
Optimal treatment settings remain a matter of debate in necessary for persistent subretinal fluid.
the reported cases. Photodynamic therapy is administered In the present study, symptomatic CCH were treated with
with intravenous verteporfin at a dose of 6 mg/m2 of body the standard PDT protocol for AMD.11 The aim of the
surface area and exposure to a laser light dose of 689 or 692 treatment was solely to achieve reabsorption of existing
nm at an intensity of 600 mW/cm2. The radiant exposure retinal detachment and improve or stabilize vision loss, but

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Ophthalmology Volume 116, Number 1, January 2009

Figure 2. Clinical appearance of the hemangioma with exudative retinal detachment affecting the fovea (arrows; patient 14). A, Superotemporal
hemangioma with exudation into the macular area. Initial visual acuity (VA) was 20/40. B, Pretreatment optical coherence tomography (OCT) shows
subretinal fluid with a height of 482 microns. C, Fundus photograph after 1 photodynamic therapy treatment shows resolution of subfoveal exudative
detachment; VA was 20/26. D, Posttreatment OCT shows restoration of the fovea and absence of subretinal fluid.

not to eliminate the tumor. After treatment, exudation dis- effusion and perifoveal hemorrhage with subsequent loss of
appeared in 93% (30/32) of tumors, cystoid macular edema VA in a patient treated with the standard AMD protocol.
was absent, VA improved in most patients, central scotomas The time interval between the diagnosis of hemangioma
disappeared, and tumor height decreased. Retreatment was when the first visual symptoms occurred and CCH treatment
performed at 3 months after the latest treatment, as was was usually long, with a mean of 24 months. Nonetheless,
done in the study of Jurklies at al.18 We believe that at- this factor did not compromise recovery of VA in this group
tempts to achieve total elimination of the tumor with this of patients, as has been reported.25 Nor did previously
treatment can lead to vascular closure of the choriocapillaris treated angiomas in our series show a significantly poorer
with consequent RPE changes. We did not observe signif- visual prognosis. Because recurrence has been observed
icant RPE changes with a radiant exposure dose of 50 J/cm2, long after treatment, a lengthier follow-up period is required
whereas Verbraak et al25 described marked RPE alterations to assess the risk of late recurrence and the long-term visual
in patients treated with a dose of 100 J/cm2. prognosis in these patients.3
In almost all the previous reports,11–15,17–29 the absence Standard AMD PDT with verteporfin resulted an effec-
of exudative retinal detachment was not confirmed by OCT. tive, minimally invasive treatment for choroidal hemangio-
Nevertheless, we believe that this technique is of great value mas with localized retinal detachment in terms of resolution
for this purpose. Even when there is an apparent absence of of exudative subretinal fluid and VA recovery in this series
subretinal fluid on fluorescein angiography, ultrasonogra- of patients. Long-term follow-up is necessary to assess
phy, and ophthalmoscopy, subretinal fluid and cystoid mac- recurrence after successful elimination of subretinal fluid.
ular edema can still be detected by OCT. In addition, with
OCT, Landau et al16 observed complete restoration of the References
foveal anatomy after treatment.
Regarding safety, there were no severe adverse events in
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3. Augsburger JJ, Shields JA, Moffat KP. Circumscribed choroi- 17. Kjeka O, Krohn J. Photodynamic therapy of circumscribed
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Ophthalmology 1994;101:1953– 61. Ophtalmol 2006;29:1013–7.
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namic therapy of experimental choroidal melanoma using the standard photodynamic treatment protocol for symptom-
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11. Treatment of Age-related Macular Degeneration with Photo- 24. Michels S, Michels R, Simader C, Schmidt-Erfurth U. Verte-
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Footnotes and Financial Disclosures


8
Originally received: March 4, 2008. Hospital La Paz, Madrid, Spain.
9
Final revision: August 10, 2008. Hospital La Fe, Valencia, Spain.
Accepted: August 12, 2008. 10
Hospital Son Dureta, Mallorca, Spain.
Available online: October 30, 2008. Manuscript no. 2008-288.
Presented in part at: American Academy of Ophthalmology, November 12,
1
Department of Ophthalmology, Hospital Vall d=Hebron, Barcelona, Spain. 2007, New Orleans, Louisiana, as a free paper (PA 067). It was given the
2
Instituto de Microcirugia Ocular, Barcelona, Spain. “Best Paper” award at the ocular tumors and pathology session.
3
Hospital Puerta de Hierro, Madrid, Spain. Financial Disclosure(s):
4 The authors have no proprietary or commercial interest in any materials
Centro de Oftalmologia Barraquer, Barcelona, Spain.
5
discussed in this article.
Instituto de Oftalmobiologia Aplicada, Valladolid, Spain.
6
Correspondence:
Hospital de Bellvitge, Hospitalet, Spain. Anna Boixadera, MD, Paseo San Gervasio 78, 5° 3a, 08022 Barcelona,
7
Hospital Conxo, Santiago de Compostela, Spain. Spain. E-mail: aboixadera@hotmail.com.

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Ophthalmology Volume 116, Number 1, January 2009

Table 2. Patient Characteristics

Duration of Tumor Height Tumor Height


Patient Symptoms VA Before VA 12-Month No. of PDT Before PDT at End
No. Age Gender (mos) Pretreatment PDT Follow-up Sessions (mm) Point (mm)
1 45 F 2005 No 20/125 20/25 1 2.6 2.22
2 65 M 2005 No 20/32 20/20 1 0.1 0.1
3 41 M 2004 No 20/160 20/100 1 4.16 1.9
4 27 M 2004 No 20/32 20/25 1 3.38 2.66
5 55 F 2005 No 20/50 20/20 1 3.5 0
6 62 F 2005 No 20/2500 20/400 1 3.98 1.84
7 32 F 2000 Laser 20/250 20/250 1 2.14 2.14
8 34 F 2004 Laser, TTT 20/125 20/250 1 4.56 1.45
9 67 M 2004 No 20/400 20/400 1 3.78 3.17
10 44 F 2004 Laser, TTT 20/200 20/50 1 2.35 1
11 43 M 2005 No 20/40 20/25 1 2.56 0.2
12 43 F 2004 No 20/20 20/20 1 5.22 1.55
13 58 M 2003 No 20/50 20/40 1 3.57 2.2
14 46 M 2003 No 20/40 20/26 1 3.57 1.04
15 54 F 2003 Laser 20/40 20/20 1 2.98 1.23
16 39 M 2000 TTT 20/20 20/20 3 2.68 1.92
17 31 M 2004 No 20/32 20/26 1 3.53 1.5
18 66 M 2005 Laser 20/50 20/20 1 2.89 2.7
19 45 F 2002 No 20/20 20/20 1 3.25 2.38
20 71 M 2003 No 20/100 20/20 1 2.8 2.43
21 61 M — No 20/200 20/125 2 3.35 2.08
22 60 M 2005 No 20/60 20/50 1 2.5 2.7
23 57 F — No 20/50 20/40 1 2.2 2
24 73 M 2005 No 20/200 20/125 1 3.29 1.45
25 40 M 2005 No 20/100 20/100 1 2.2 1.2
26 21 M 2004 No 20/125 20/125 2 3.1 2.9
27 59 M 2004 No 20/100 20/30 1 2.3 1.4
28 51 M 2004 No 20/400 20/400 1 1.8 0
29 20 F 2002 TTT 20/26 20/20 2 2.32 2.05

F ⫽ female; M ⫽ male; PDT ⫽ photodynamic therapy; TTT ⫽ transpupillary thermotherapy; VA ⫽ visual acuity.

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