Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Evaluation of Choroidal Hemangioma and Treatment With Photodynamic Therapy by Using Enhanced Depth Imaging Optical Coherence Tomography

Zeynep Gursel Ozkurt, MD; Naziha Slimani, MD; Hakan Demirci, MD

Abstract

This article has been amended to include factual corrections. To read the erratum, click here. The online article and its erratum are considered the version of record.

BACKGROUND AND OBJECTIVE:

To evaluate enhanced depth imaging optical coherence tomography (EDI-OCT) features of choroidal hemangioma and changes following photodynamic therapy (PDT).

PATIENTS AND METHODS:

Retrospective review of 21 choroidal hemangiomas.

RESULTS:

On EDI-OCT, choroidal hemangioma showed low internal reflectivity in 47% of lesions and high internal reflectivity in 53%. The most common associated features were normal-looking honeycomb-like pattern in choriocapillaris in all lesions, inner segment/outer segment abnormality in 62%, photoreceptor outer segment abnormality in 62%, subretinal fluid with speckles in 62%, and shaggy photoreceptors in 57% of lesions. Internal reflectivity changed from low to high in 67% of lesions. Photoreceptor outer segment and plexiform layer abnormalities became more noticeable and shaggy photoreceptors improved.

CONCLUSION:

On EDI-OCT, choroidal hemangioma showed normal-looking honeycomb-like pattern in the choriocapillaris, subretinal fluid with speckles, and abnormalities in the photoreceptor outer segment and plexiform layers. Following PDT, the choriocapillaris became sclerotic, and photoreceptor outer segment layer abnormalities were prominent.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:171–178.]

Abstract

This article has been amended to include factual corrections. To read the erratum, click here. The online article and its erratum are considered the version of record.

BACKGROUND AND OBJECTIVE:

To evaluate enhanced depth imaging optical coherence tomography (EDI-OCT) features of choroidal hemangioma and changes following photodynamic therapy (PDT).

PATIENTS AND METHODS:

Retrospective review of 21 choroidal hemangiomas.

RESULTS:

On EDI-OCT, choroidal hemangioma showed low internal reflectivity in 47% of lesions and high internal reflectivity in 53%. The most common associated features were normal-looking honeycomb-like pattern in choriocapillaris in all lesions, inner segment/outer segment abnormality in 62%, photoreceptor outer segment abnormality in 62%, subretinal fluid with speckles in 62%, and shaggy photoreceptors in 57% of lesions. Internal reflectivity changed from low to high in 67% of lesions. Photoreceptor outer segment and plexiform layer abnormalities became more noticeable and shaggy photoreceptors improved.

CONCLUSION:

On EDI-OCT, choroidal hemangioma showed normal-looking honeycomb-like pattern in the choriocapillaris, subretinal fluid with speckles, and abnormalities in the photoreceptor outer segment and plexiform layers. Following PDT, the choriocapillaris became sclerotic, and photoreceptor outer segment layer abnormalities were prominent.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:171–178.]

Introduction

Diagnosis of circumscribed choroidal hemangioma could be challenging in some patients. The classical features of orange colored mass on fundus examination, acoustic solidity and high internal reflectivity on B- and A-scan ultrasonography, and late “wash-out” hypofluorescence on the late phase of indocyanine green angiography might not be enough for diagnosis. In a review of 200 circumscribed choroidal hemangiomas, Shields et al. reported that 38% of cases were initially diagnosed as choroidal melanoma or metastasis before referral to the ocular oncology center.1

With axial resolution up to 5 μm and its ability to image the morphologic structure of choroid, enhanced depth imaging using enhanced depth imaging optical coherence tomography (EDI-OCT) has become another useful diagnostic tool. Following the first report by Torres et al., EDI-OCT features of various choroidal tumors have been reported in the literature.2–5 Anterior tumor surface features like “lumpy bumpy” appearance in choroidal metastasis, “seasick” surface in lymphoma, and “rocky and rolling” configuration in sclerochoroidal calcification have been described in the differential diagnosis of choroidal tumors. Previously, Rojanaporn et al. reviewed EDI-OCT features in 10 circumscribed choroidal hemangiomas and observed gently sloping choroidal mass with expansion of medium- and large-sized choroidal vessels without compression of the choriocapillaris.6 Photodynamic therapy (PDT) is the most common treatment for circumscribed choroidal hemangiomas.7–9 It has been used in diffuse or circumscribed choroidal hemangiomas as monotherapy or in combination with intravitreous bevacizumab (Avastin; Genentech, South San Francisco, CA).10–13 There is limited information about the post-PDT changes in retinal and choroidal layers. In this study, we retrospectively evaluated the EDI-OCT features in 21 circumscribed choroidal hemangiomas and the changes in these features following PDT in eight patients.

Patients and Methods

Following institutional review board approval, we retrospectively analyzed the clinical and EDI-OCT features of 21 consecutive patients with choroidal hemangioma managed in the Ocular Oncology Clinic, Department of Ophthalmology and Visual Sciences, University of Michigan, W.K. Kellogg Eye Center between May 2011 to July 2015.

The EDI-OCT was performed by using Spectralis HRA + OCT (Heidelberg Engineering, Heidelberg, Germany) using acquisition and analysis software. The images were obtained using an image acquisition protocol of 13 raster lines of 9-mm image length, with 1,536 A-scans per line and automatic real-time averaging set at 100 images.

Age, gender, and clinical data — including location of the epicenter of the hemangioma, basal diameters (millimeters), associated subretinal fluid, RPE changes, subretinal fibrosis, and drusen — were recorded. EDI-OCT images were analyzed for features of the hemangioma including: thickness (μm), configuration, optical shadowing, optical reflectivity, and changes in choriocapillaries. Overlying retina, Bruch's membrane, and retinal pigment epithelium (RPE) were also evaluated. Thickness of the hemangioma was measured by placing the calipers at the echogenic spikes corresponding to the tumor apex and scleral base in ultrasonography (μm) by two independent observers (ZO, NS). Similarly, in EDI-OCT (μm), the calipers were placed anteriorly at the base of RPE and posteriorly at the tumor base at the scan, when visible, showing the greatest tumor thickness by two independent observers (ZO, NS). Choriocapillaris thickness is estimated by placing the calipers at the base of RPE and at the top of the tumor at the highest tumor thickness. Intratumoral vessel diameter is estimated by picking the biggest tumor vessel at the highest tumor thickness and placing the calipers at the walls of the vessel.

Eight patients received PDT. After informed consent a dose of 6 mg/m2 of verteporfin (Visudyne; Novartis AG, Basel, Switzerland) was infused intravenously during the course of 10 minutes. After a 5-minute delay, the patient was brought to the laser slit-lamp, where a contact lens was placed on the eye. Using fluorescein guidance, the spot was placed over the hemangioma with 1 mm margin and 600 mW/cm power was applied to the lesion for 83 seconds with light dose at 689 nm. Tumor features at the clinical examination, ultrasonography, and EDI-OCT were analyzed after at least one PDT session.

Statistical calculations were performed using the SPSS 15.0 statistical package (SPSS, Chicago, IL). All data are presented as mean and range. Nonparametric tests were used for statistical analyses. Before and after PDT measurements were compared with Wilcoxon signed-ranks test. A P value less than .05 was regarded as statistically significant.

Results

Of 21 patients, 12 (57%) were male and nine (43%) were female. The mean age of patients was 54 years (median: 55 years; range: 9 years to 81 years). Clinical features of these patients are presented in Table 1. The mean thickness of choroidal hemangioma was 2,390 μm (median: 1,800 μm; range: 1,500 μm to 2,400 μm) by ultrasonography and 1,519 μm (median: 1,372 μm; range: 1,150 μm to 1,700 μm) by EDI-OCT. In seven patients with visible posterior border on EDI-OCT, the mean difference in tumor thickness measured by ultrasonography versus EDI-OCT was 514 μm (P < .05). EDI-OCT features of choroidal hemangioma are shown in Table 2. In choriocapillaris, honeycomb-like vascular pattern was observed in all 21 hemangiomas (Figures 1A–1C). The mean estimated overlying choriocapillaris thickness was 204 μm (range: 80 μm to 305 μm). The mean estimated intratumoral vessel diameter was 338 μm (range: 225 μm to 459 μm) and normal choroid vessel diameter was 232 μm (range: 194 μm to 282 μm). Estimated intratumoral vessel diameters were significantly larger than normal choroid vessel diameters (P < .001).

Clinical Features of 21 Choroidal Hemangiomas

Table 1:

Clinical Features of 21 Choroidal Hemangiomas

Enhanced Depth Imaging Optical Coherence Tomography Features of 21 Choroidal Hemangiomas

Table 2:

Enhanced Depth Imaging Optical Coherence Tomography Features of 21 Choroidal Hemangiomas

(A) Choroidal hemangioma on the macula causing decreased vision. (B, C) On enhanced depth imaging optical coherence tomography, normal-looking honeycomb-like choriocapillaris (asterisk), overlying subretinal fluid, and exudates (arrow) are visible. (D, E) After photodynamic therapy, the choriocapillaris showed normal-looking honeycomb-like pattern with sclerosis (asterisk). Subretinal fluid improved.

Figure 1.

(A) Choroidal hemangioma on the macula causing decreased vision. (B, C) On enhanced depth imaging optical coherence tomography, normal-looking honeycomb-like choriocapillaris (asterisk), overlying subretinal fluid, and exudates (arrow) are visible. (D, E) After photodynamic therapy, the choriocapillaris showed normal-looking honeycomb-like pattern with sclerosis (asterisk). Subretinal fluid improved.

(A) A choroidal hemangioma inferior to the optic disc. (B) Enhanced depth imaging optical coherence tomography showed normal-looking honeycomb-like choriocapillaris (asterisk) and abnormalities in the outer photoreceptor and plexiform layer (arrow).

Figure 2.

(A) A choroidal hemangioma inferior to the optic disc. (B) Enhanced depth imaging optical coherence tomography showed normal-looking honeycomb-like choriocapillaris (asterisk) and abnormalities in the outer photoreceptor and plexiform layer (arrow).

(A) A choroidal hemangioma along the superotemporal arcade. (B) On enhanced depth imaging optical coherence tomography, normal-looking honeycomb-like choriocapillaris (asterisk) with abnormalities in the outer photoreceptor and plexiform layers (arrow).

Figure 3.

(A) A choroidal hemangioma along the superotemporal arcade. (B) On enhanced depth imaging optical coherence tomography, normal-looking honeycomb-like choriocapillaris (asterisk) with abnormalities in the outer photoreceptor and plexiform layers (arrow).

(A) A choroidal hemangioma on the macula. (B) Normal-looking honeycomb-like choriocapillaris (asterisk) with overlying intraretinal fluid (arrow) were visible on enhanced depth imaging optical coherence tomography.

Figure 4.

(A) A choroidal hemangioma on the macula. (B) Normal-looking honeycomb-like choriocapillaris (asterisk) with overlying intraretinal fluid (arrow) were visible on enhanced depth imaging optical coherence tomography.

Eight patients were treated with PDT. The number of sessions was one for five patients, two for two patients, and five for one patient. The mean time of follow up since the first PDT session was 23 months (range: 4 months to 70 months). Following the PDT, EDI-OCT features are evaluated. In these eight patients, the pretreatment mean thickness was 2,363 μm by ultrasonography and 1,371 μm by EDI-OCT. The post-treatment mean thickness was 1,613 μm by ultrasonography and 997 μm by EDI-OCT. After the PDT, the mean decrease in the thickness of choroidal hemangioma was 374 μm (range: 96 μm to 976 μm) by EDI-OCT and 750 μm (range: 300 μm to 1,800 μm) by ultrasonography (P = .007 and P = .02 respectively). This corresponded 26% mean decrease in thickness by EDI-OCT and 33% mean decrease by ultrasonography. The internal optical reflectivity changed from low reflective to high reflective in six patients (75%) and remained low reflective in two patients (25%). Normal-looking honeycomb-like pattern in the choriocapillaris remained the same in all our patients. (Figures 1D and 1E) Changes in EDI-OCT features in retina layers following the PDT are presented in Table 3. After the PDT, the mean estimated overlying choriocapillaris thickness decreased from 157 μm (range: 80 μm to 222 μm) to 103 μm (range: 56 μm to 167 μm), the mean estimated intratumoral vessel diameter decreased from 366 μm (range: 284 μm to 459 μm) to 284 μm (range: 154 μm to 424 μm), and the decreases were statistically significant (P = .012 and P = .017, respectively).

Retinal Layer Abnormalities Before and After Photodynamic Therapy

Table 3:

Retinal Layer Abnormalities Before and After Photodynamic Therapy

Choroidal Hemangioma Thicknesses on Ultrasound and EDI-OCT Before and After PDT

Table 4:

Choroidal Hemangioma Thicknesses on Ultrasound and EDI-OCT Before and After PDT

(A) A choroidal hemangioma on the macula. (B) On enhanced depth imaging optical coherence tomography, normal-looking honeycomb-like choriocapillaris (asterisk) with overlying retinal pigment epithelium, outer photoreceptor, and plexiform layer abnormalities are visible (arrow).

Figure 5.

(A) A choroidal hemangioma on the macula. (B) On enhanced depth imaging optical coherence tomography, normal-looking honeycomb-like choriocapillaris (asterisk) with overlying retinal pigment epithelium, outer photoreceptor, and plexiform layer abnormalities are visible (arrow).

Discussion

On EDI-OCT, different choroidal tumors show certain anterior tumor surface and intrinsic tumor structure features. In a review of EDI-OCT features of 104 choroidal nevi, Shah et al. found that 63% had dome shape and 94% had compression of overlying choriocapillaris.14 Shields et al. imaged 37 small choroidal melanomas with EDI-OCT and observed that 92% had dome shape and 100% had compression of choriocapillaris.15 Previously, we reported that plateau-shaped tumor elevation (elevated tumor with flat, wavy RPE apical surface) in 75% of metastatic choroidal metastasis and thinning of choriocapillaris over the metastatic tumor in all of them.5 Choroidal lymphoma, another differential diagnosis of amelanotic choroidal lesions, was reported to show smooth (calm), mini-wavy (rippled) or maxi-wavy (undulating) anterior surface in 50%, 15%, and 35% of cases, respectively, correlating with increasing tumor thickness and inward compression of choroidal vascular structures.16

In a review of EDI-OCT features of different choroidal tumors, Torres et al, showed medium to low reflective band with a homogeneous signal and intrinsic spaces corresponding to inner vascular spaces in three circumscribed choroidal heangiomas.2 Later, Rojanaporn et al. analyzed EDI-OCT features in 10 circumscribed choroidal hemangiomas and found that all had a smooth with a gently sloping anterior contour, and expansion of medium and large size choroidal vessels without compression of choriocapillaris.6 In a recent study of en face mode of swept-source OCT, circumscribed choroidal hemangioma was imaged as hyporeflective, confluent, oval or round areas, corresponding with the lumen of the tumor vascular spaces and hyperreflective zones. These hyperreflective areas were thought to represent the vessel walls and surrounding connective tissue and were observed to increase from inner to outer zones.17 In our study, 95% of circumscribed choroidal hemangiomas had dome shape and all of them showed normal-looking honeycomb-like pattern in the choriocapillaris layer. We observed that choroidal vessels are diffusely enlarged in the outer most Haller's and middle Sattler's layers without compression of choriocapillaris. Intratumor vessel diameter were significantly increased, when compared to normal choroidal vessels.

In a histopathological review of circumscribed choroidal hemangiomas, Witschel and Font showed that choroidal hemangiomas were classified as predominantly capillary composed of small, capillary-type vessels lined by flat, inconspicuous endothelial cells, and predominantly cavernous, consisted of large, thin-walled, blood channels lined by a flat endothelium. There was thin, loose connective tissue between blood vessels in both types.18 Fibrous plaque and ossification covering inner surface of the choroid were observed in 69% and 11% of circumscribed choroidal hemangiomas, respectively. They found no vascular involvement, but obliteration and sclerosis in the choriocapillaris. There was mild atrophy to focal proliferation with drusen formation in the overlying retinal pigment epithelium. In the retina, there are loss of photoreceptors, severe cystoid degeneration of the outer layers and marked gliosis. Similarly, in EDI-OCT, we observed that choriocapillaris and anterior part of Sattler's layer were uninvolved with intrinsic obliteration and sclerosis that gives the honeycomb appearance. The overlying fibrosis or poor penetration of infrared light through fluid and blood might explain why the vascular details are not visible in some cases. RPE changes were present in 35% of cases, as well as photoreceptor outer segment abnormalities in 60% of cases.

Post-PDT changes in OCT features of circumscribed choroidal hemangioma have not been described in detail. Shinojima et al. reviewed morphologic alterations in spectral-domain OCT after PDT in idiopathic central serous chorioretinopathy and reported visible inner and outer segment junction line in 76% of eyes, and RPE irregularities in all eyes.19 Similarly, we observed that abnormalities in photoreceptor outer segment and outer plexiform layer increased following PDT. In the choroid layer, there was an increase in obliteration and sclerosis of choriocapillaris and decrease in the diameter of choroidal vessels. Scholtzer-Schrehardt et al. showed the closure of choriocapillaris by sparing deeper layers of choroid, retina, and RPE in the histological examination of eyes that underwent PDT.20 They claimed that the blood supply from the deeper choroidal layer preserved the retinal layers. In circumscribed choroidal hemangioma, the closure of the larger vessels as well as choriocapillaris might lead to retinal and RPE changes.

Thickness of choroidal lesions was less when measured with EDI-OCT than ultrasonography.14,15,21 This was explained by the low resolution of ultrasonography and poor differentiation of the retina and sclera in the ultrasonography, but other factors related to each imaging technology might play a role in the difference. We measured that the hemangioma thickness was 27% less when measured with EDI-OCT. The difference in hemangioma thickness measurement became more prominent in lesions with subretinal fluid. It was reported 70% in the literature and 38% in our study.6 Similarly, following treatment, the mean decrease in hemangioma thickness was more in the ultrasonography, probably due to the more specific measurement of choroidal hemangioma in EDI-OCT, and resolution of subretinal or intraretinal fluid.

In summary, low internal reflectivity, large choroidal vessels, and normal-looking honeycomb-like pattern in choriocapilaris and anterior part of Sattler's layer were common EDI-OCT imaging features of choroidal hemangioma. Following PDT, choroidal and intratumoral vessel diameter decreased. Abnormalities in photoreceptor outer segment and outer plexiform layer abnormalities became noticeable, and shaggy photoreceptors improved.

References

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Clinical Features of 21 Choroidal Hemangiomas

Clinical Features Patient Number (%)

Location of Tumor Epicenter
  Macula 5 (24)
  Superior 12 (57)
  Inferior 3 (14)
  Nasal 1 (1)

Tumor Basal Diameter, mm
  Mean 9.2
  Median 8.0
  Range 6–15

Tumor Thickness on Ultrasonography, mm
  Mean 2.4
  Median 2.3
  Range 1.5–4.6

Configuration on Ultrasonography
  Oblong 12 (57)
  Dome 9 (43)

Associated Findings on Examination
  Subretinal fluid 13 (62)
  Retina pigment epithelium changes 7 (33)
  Subretinal fibrosis 4 (19)
  Drusen 2 (9)

Enhanced Depth Imaging Optical Coherence Tomography Features of 21 Choroidal Hemangiomas

EDI-OCT Features Patient Number (%)

Configuration
  Dome 20 (95)
  Plateau 1 (5)

Optical Shadowing
  Complete 5 (24)
  Partial 16 (76)

Optical Reflectivity
  Low optical reflection 10 (57)
  High optical reflection 11 (48)

Associated Findings
  Bruch membrane thickening/atrophy 2 (9)
  RPE thickening/atrophy 8 (38)
  Photoreceptor outer segment abnormality 13 (62)
  Inner segment-outer segment abnormality 13 (62)
  External liming membrane abnormality 8 (38)
  Outer nuclear layer abnormality 6 (28)
  Outer plexiform layer abnormality 6 (28)
  Inner nuclear layer abnormality 7 (33)
  Inner plexiform layer abnormality 5 (24)
  Ganglion cell layer abnormality 6 (28)
  Nerve fiber layer abnormality 6 (28)
  Shaggy photoreceptor (elongated and swollen) 12 (57)
  Subretinal fluid with speckles 15 (71)
  Intraretinal fluid 6 (28)

Retinal Layer Abnormalities Before and After Photodynamic Therapy

EDI-OCT Features Before PDT Patient Number (%) After PDT Patient Number (%)
Bruch's membrane thickening/atrophy 1 (13) 0 (0)
RPE thickening/atrophy 4 (50) 5 (63)
Photoreceptor outer segment abnormality 3 (37) 5 (63)
Inner segment-outer segment abnormality 6 (75) 5 (63)
External limiting membrane abnormality 4 (50) 5 (63)
Outer nuclear layer abnormality 3 (37) 4 (50)
Outer plexiform layer abnormality 1 (13) 4 (50)
Inner nuclear layer abnormality 3 (37) 2 (25)
Inner plexiform layer abnormality 1 (13) 2 (25)
Ganglion cell layer abnormality 2 (25) 3 (37)
Nerve fiber layer abnormality 2 (25) 3 (37)
Shaggy photoreceptor (elongated & swollen) 5 (63) 2 (25)
Subretinal fluid with speckles 8 (100) 5 (63)
Intraretinal fluid 4 (50) 4 (50)

Choroidal Hemangioma Thicknesses on Ultrasound and EDI-OCT Before and After PDT

Measurement Method Mean Tumor Thickness Before PDT Mean Tumor Thickness After PDT Mean Decrease in Thickness P Value
Ultrasonography 2,363 μm (range: 1,800 μm to 2,800 μm) 1,613 μm (range: 0 μm to 2,500 μm) 750 μm (range: 300 μm to 1,800 μm) .007
EDI-OCT 1,371 μm (range: 1,150 μm to 1,451 μm) 997 μm (range: 359 μm to 1,450 μm) 374 μm (range: 96 μm to 976 μm) .02
Authors

From Ocular Oncology, University of Michigan Department of Ophthalmology and Visual Sciences, W.K. Kellogg Eye Center, Ann Arbor, MI.

The authors report no relevant financial disclosures.

The authors would like to thank Mr. and Mrs. Witham for their generous support of this paper.

Address correspondence to Hakan Demirci, MD, W.K. Kellogg Eye Center, University of Michigan, 1000 Wall Street, Ann Arbor, MI 48105; email: hdemirci@umich.edu.

Received: May 02, 2017
Accepted: October 05, 2017

10.3928/23258160-20180221-04

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