Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Efficacy of Retinal Lesion Screening in Von Hippel-Lindau Patients With Widefield Color Fundus Imaging Versus Widefield FA

Liliya Golas, MD; Dimitra Skondra, MD, PhD; Shaun Ittiara, MD; Nicole Bajic, MD; Karen W. Jeng-Miller, MD, MPH; Shizuo Mukai, MD; Yoshihiro Yonekawa, MD; Michael P. Blair, MD

Abstract

BACKGROUND AND OBJECTIVE:

Retinal hemangioblastoma is a retinal tumor in patients with Von Hippel-Lindau (VHL). The authors' objective was to determine whether widefield fluorescein angiography (FA) improves lesion detection.

PATIENTS AND METHODS:

Retrospective case series of VHL patients who underwent widefield fundus imaging and FA. Masked retina specialists graded fundus images as having: 1) definite retinal hemangioblastoma; 2) possible lesion; 3) no lesion. The number of lesions on FA was compared to widefield color imaging.

RESULTS:

One hundred six eyes of 55 patients were evaluated. A total of 94 lesions were identified on FA in 61.8% patients. Forty-three lesions (45.7%) were not identified on fundus images. Small lesion detection was significantly higher with FA compared to color imaging (P = .013).

CONCLUSIONS:

This study reports on improved detection of retinal hemangioblastomas with widefield FA compared to widefield fundus images. The authors recommend VHL monitoring guidelines to include periodic widefield FA to adequately screen for smaller lesions.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:e260–e265.]

Abstract

BACKGROUND AND OBJECTIVE:

Retinal hemangioblastoma is a retinal tumor in patients with Von Hippel-Lindau (VHL). The authors' objective was to determine whether widefield fluorescein angiography (FA) improves lesion detection.

PATIENTS AND METHODS:

Retrospective case series of VHL patients who underwent widefield fundus imaging and FA. Masked retina specialists graded fundus images as having: 1) definite retinal hemangioblastoma; 2) possible lesion; 3) no lesion. The number of lesions on FA was compared to widefield color imaging.

RESULTS:

One hundred six eyes of 55 patients were evaluated. A total of 94 lesions were identified on FA in 61.8% patients. Forty-three lesions (45.7%) were not identified on fundus images. Small lesion detection was significantly higher with FA compared to color imaging (P = .013).

CONCLUSIONS:

This study reports on improved detection of retinal hemangioblastomas with widefield FA compared to widefield fundus images. The authors recommend VHL monitoring guidelines to include periodic widefield FA to adequately screen for smaller lesions.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:e260–e265.]

Introduction

Von Hippel-Lindau (VHL) syndrome is a rare, inherited disorder resulting in the formation of neoplasms of multiple organ systems. Although the syndrome is most commonly characterized by hemangioblastomas of the retina, brain, and spinal cord, other associated neoplasms can include renal cell carcinoma, pheochromocytoma, and cysts of the pancreas, kidneys, epididymis, or broad ligaments.1,2 VHL is an autosomal dominant condition caused by mutations in the VHL tumor suppressor gene on chromosome 3.3–5 Although the overall incidence is low, about one in every 36,000 live births, the disease has high penetrance, with 95% of those with a VHL mutation having at least one of the aforementioned tumors by the age of 60.6,7

Retinal capillary hemangioblastoma (RCH) is the most common and earliest VHL manifestation, reported in 49% to 85% of patients.6–9 The lesion is often described as a well-circumscribed, orange-red globular retinal mass with dilated and tortuous feeding artery and draining vein (Figure 1). Advanced lesions can lead to vision loss due to exudation, macular edema, retinal detachment, and extensive scarring.8–13 Typically, the average age at first detection of an RCH in VHL patients is 25 years. However, it can occur in the pediatric population, as well, with a reported incidence of 5% in patients younger than 10 years of age.8 Furthermore, younger patient age at the time of diagnosis is associated with greater risk of vision loss. Additionally, an increased risk of vision loss is also associated with juxtapapillary location of RCHs and increased number of peripheral RCHs.12 There is a life-long risk of developing new RCHs in VHL patients.

Widefield fundus photo of a large retinal hemangioblastoma with surrounding exudates and subretinal fluid.

Figure 1.

Widefield fundus photo of a large retinal hemangioblastoma with surrounding exudates and subretinal fluid.

Current VHL surveillance guidelines recommend only annual dilated fundus exam (DFE) by an ophthalmologist for VHL patients or “at-risk” relatives who have yet to obtain genetic testing starting at 1 year of age.1,14 Unfortunately, small lesions may be difficult to detect on DFE or fundus photography alone and timely detection and treatment of these lesions may be delayed. Conventional fundus cameras can image 30° to 50° of the retina in a single capture, which increases to about 75° with using the Diabetic Retinopathy Study seven standard field protocol. With the use of widefield imaging, we are now able to image up to 200° (or 85%) of the retina in single capture, which increases even more with gaze steering at the time of the test.15 Schoen et al. report a case with clinically invisible RCHs that were detected with fluorescein angiography (FA).16 A recent report of a small case series of 10 patients by Chen et al. has further lent credence to the advantage of widefield FA in detecting early retinal angiomas not visible on conventional FA, indirect ophthalmoscopy, or fundus photographs.17

Treatment of VHL-related RCHs is guided by the lesion location, size, and the presence or absence of subretinal fluid, retinal traction, or retinal detachment. Laser photocoagulation, with either argon or diode laser, has emerged as a favored option in smaller lesions amenable to laser therapy.10,18–24 Lesion growth over time and greater chance of successful treatment with small lesions makes early detection important in order to perform early treatment or at least frequent monitoring.

The purpose of this study is to investigate the detection rate of VHL lesions with widefield angiography compared to widefield color imaging. We aim to determine whether widefield FA improves detection of retinal lesions in VHL patients and how that correlates with parameters of lesion location and size.

Patients and Methods

This is a retrospective case series of patients with genetically confirmed VHL diagnosis who underwent widefield fundus color imaging and widefield FA at the University of Chicago Ophthalmology Clinic and the Massachusetts Eye and Ear Infirmary. The study protocol was approved by the local Institutional Review Board of the University of Chicago and Massachusetts Eye and Ear Infirmary, and the study was conducted in accordance with the Declaration of Helsinki.

Data obtained from retrospective chart review included results of genetic testing, systemic manifestations of VHL, visual acuity at clinical presentation, age at time of ophthalmic imaging, interpretations of widefield color fundus imaging and widefield FA, and whether treatment of any present lesions was performed. Imaging was obtained using the Optos 200Tx (Optos, Dunfermline, United Kingdom) by an ophthalmic photographer. Inclusion criteria for the study included a diagnosis of VHL with at least one ophthalmic examination as well as at least one widefield color fundus imaging and widefield FA obtained. Exclusion criteria included a lack of widefield fundus photos and FA, images obtained with other cameras, the presence of non-angiomatous retinal lesions and/or masses, or a history of treated lesions without subsequent new lesions since treatment or without photos from prior to treatment. On this basis, 16 patients were excluded from our study, with one patient being excluded due to concurrent retinoblastoma.

Masked retina specialists (YY, SI) reviewed the color fundus images and graded them as having: 1) definite retinal hemangioblastoma; 2) possible lesion; 3) no lesion. Lesion location (anterior or posterior to equator and lesion quadrant) and size (0.25 disc diameter [DD] or less, more than 0.25 DD to 0.5 DD, more than 0.5 DD to 1 DD, or more than 1 DD) were also recorded. Widefield fluorescein angiograms were graded the same way, and consequently comparison of the number and characteristics of lesions identified with either modality was performed. Fisher's exact test was used for comparison of lesions detected with FA vs color images (GraphPad Software, 2018; GraphPad, San Diego, CA). A P value of less than .05 was considered to be statistically significant.

Results

We evaluated 106 eyes of 55 patients with genetically confirmed VHL. All 55 patients had at least one widefield FA as well as widefield fundus images obtained during the past 6 years. Mean age of the VHL patients studied was 30 years, ranging from 14 months to 68 years. Thirty-seven of the patients (67%) were female. We did not find any correlations between RCH number/size/location and specific VHL mutation.

On widefield FA, 94 lesions in 44 eyes of 34 patients (61.8%) were identified. Fifteen eyes (35%) had two or more lesions. Bilateral RCHs were found in 10 patients (29.4%). Most of the lesions were found in peripheral retina, with 74% of them being anterior to the equator. Additionally, 64 lesions (65%) were 0.25 DD or smaller in size. Only 21 lesions were larger than 1 DD in size.

Of the 94 identified lesions on widefield FA, 43 (45.7%) lesions in 26 eyes were missed on fundus photographs (Table 1). Of these missed lesions, 81% were anterior to the equator and 83.7% were 0.25 DD in size or smaller. Table 2 shows the distribution of missed lesion size and quadrant. However, for 15 of the missed lesions, the corresponding fundus photograph did not extend as far into the periphery as on FA and were therefore excluded from statistical analysis. Additionally, a total of seven eyes had erroneous lesions identified, with graders identifying possible lesions on photographs that were not confirmed on FA.

Distribution of Lesions Identified on Widefield Color Fundus Imaging Compared toWidefield Fluorescein Angiography

Table 1:

Distribution of Lesions Identified on Widefield Color Fundus Imaging Compared toWidefield Fluorescein Angiography

Missed Lesion Characteristics Based on Size and Quadrant

Table 2:

Missed Lesion Characteristics Based on Size and Quadrant

Including only those lesions identified on FA in areas imaged on fundus images, a significantly higher number of small lesions were detected on widefield FA compared to color fundus imaging (P = .013, Fisher's exact test, two-tailed) (Table 3).

Comparison of Lesions Identified on Widefield Color Imaging VersusWidefield Fluorescein Angiography

Table 3:

Comparison of Lesions Identified on Widefield Color Imaging VersusWidefield Fluorescein Angiography

Two masked retina specialists graded the widefield color fundus images, one at the University of Chicago and the other at the Massachusetts Eye and Ear Infirmary. Percentage of lesions missed by each grader was not significantly different (9/39 (23.1%) vs. 19/55 (34.5%), respectively; P = .51, two-tailed).

Discussion

Retinal hemangioblastomas are the most common VHL manifestation and if left untreated may lead to profound vision loss. Current surveillance guidelines for VHL patients are rather vague, with only annual DFE recommendation, and do not include the use of newer imaging modalities that are available in many retina clinics at this time.14 Although larger lesions are generally easily identified on clinical examination, smaller lesions may be difficult to detect on routine DFEs and even widefield photography alone (Figure 2). In the current study, we have demonstrated a significantly higher rate of detection of these small lesions with FA compared to color fundus imaging. With widefield FA as used in the present study, smaller peripheral lesions that may not be visible on routine exams or fundus photography may be found sooner, allowing for earlier, less-invasive treatment with laser photocoagulation, which has minimal side effects and may halt progression of the lesions before vision loss occurs. Kim et al. showed that treated lesions smaller than 0.5 mm in diameter had complete regression in 90% of cases, compared to 67% for tumors 3.0 mm or larger.23 Furthermore, eye exams may be even more difficult in pediatric patients, further delaying early treatment of these lesions in children. We recommend starting screening with widefield FAs at the time of diagnosis and then periodically, including in pediatric patients. To minimize potential side effects of intravenous fluorescein and possible need for sedation, oral fluorescein can be considered in these patients. Understanding the potential anesthesia risks in pediatric patients, it would be wise to attempt to combine any necessary testing and treatments in a multidisciplinary approach.

Retinal hemangioblastoma missed on widefield fundus photo (A) but readily visible on widefield fluorescein angiogram (B), allowing early laser photocoagulation treatment (C).

Figure 2.

Retinal hemangioblastoma missed on widefield fundus photo (A) but readily visible on widefield fluorescein angiogram (B), allowing early laser photocoagulation treatment (C).

In our study, we compared the number of lesions detected on widefield FAs to those identified on fundus photographs instead of clinical exams. The rate of detection on clinical exam may be higher, lower, or the same as on widefield fundus photographs, depending on the ophthalmologist and the patient, but likely worse than fluorescein angiograms. The use of widefield FA has been shown to improve detection of peripheral retinal lesions that may be missed on DFEs or conventional imaging in diabetic retinopathy and sickle cell retinopathy, as well as VHL.16,17,25,26 In our study, 45.7% of lesions detected on widefield FAs were not visible on fundus photography, which is similar to 45% of eyes with missed lesions compared to clinical exams reported by Chen et al.17 in a smaller study. We chose to compare photographs, rather than clinical exam, with FA, because with the retrospective study design, the majority of the clinical exams were performed at the same visit as the widefield FAs, potentially introducing bias into the recording of the findings of DFEs in clinical charts. In our study, the retina specialists grading the photographs were masked to the patients' recorded clinical exams to eliminate this bias. One of the limitations of our study is that each grader evaluated the set of images obtained at their institution; therefore, we are unable to evaluate intergrader variability for the same patients. However, the percentage of missed lesions did not statistically differ between the graders. Additionally, retrospective design is another limitation of our study, but because VHL is such a rare disease, prospective study comparing clinical exam to widefield imaging would be difficult to accomplish with similar number of patients we were able to analyze in our study.

The use of widefield systems has its limitations as well. If not performed correctly, there may be significant peripheral distortion and obstruction from artifact/eyelids/eyelashes. Even though widefield systems allow for up to 82% of the retina to be imaged with single capture, the remaining peripheral retina may harbor additional lesions. This can be mitigated by obtaining additional images with gaze steering and eyelid retraction to minimize obstruction and increase the viewing angle. Patients with limited cooperation with widefield imaging will likely have even greater difficulties cooperating with a thorough dilated eye exam, which requires significantly brighter lights than those required for Optos widefield imaging. In our study, for 15 of the missed lesions, the corresponding color photograph quadrants evaluated did not extend as far in the periphery or the lesions were obstructed by artifact in the photos compared to FA. Photographers obtaining widefield FAs are more likely to take additional images with gaze steering or lid retraction if there are possible lesions seen at the time of the test, likely even further increasing the rate of detection compared to photographs.

It is well-known that FA is an invasive test that requires venipuncture and has potential complications and side effects, ranging from nausea and vomiting to itching, hives, and even anaphylaxis.27–30 However, the more serious complications are reported in only up to 0.3% of patients,30 and most studies well under 0.1%. Risks, benefits, and alternatives should be discussed with patients prior to performing the test, and the patient's prior adverse reactions should be considered prior to repeating FA testing.

In conclusion, smaller retinal hemangioblastomas may not be visible on DFE or fundus photography, and some will be missed without widefield FA. We recommend screening of patients with VHL to continue to include annual dilated exams but with the addition of widefield FA at initial presentation, and then periodically due to lifelong risk of lesion development, to improve early detection of smaller lesions, allowing for less invasive treatment and prevention of significant vision loss.

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Distribution of Lesions Identified on Widefield Color Fundus Imaging Compared toWidefield Fluorescein Angiography

Lesions Identified on Fundus Imaging as Compared to Fluorescein Angiography (n)% Anterior to Equator% 0.25 DD Size or Smaller
Missed (43)8183.7
Possible (8)37.587.5
Definite (43)74.432.6

Missed Lesion Characteristics Based on Size and Quadrant

Lesion CharacteristicsMissed Lesions, N (%)
≤ 0.25 DD30 (70)
> 0.25–0.5 DD11 (26)
> 0.5–1 DD1 (0.2)
> 1 DD1 (0.2)
Temporal13 (30)
Nasal6 (14)
Superior8 (19)
Inferior16 (37)

Comparison of Lesions Identified on Widefield Color Imaging VersusWidefield Fluorescein Angiography

Lesions Identified OnColorFA
≤ 0.25 DD1751
> 0.25 DD2628
PValue.013(Fisher's exact test, two-tailed)
Authors

From the Department of Ophthalmology, University of Chicago, Chicago (LG, DS, NB, MPB); Retinal Vitreal Consultants, LTD, Chicago (SI); the Department of Ophthalmology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston (KJM, SM); Pediatric Retina Service, Boston Children's Hospital, Harvard Medical School, Boston (KJM, SM); and Wills Eye Hospital Retina Service, Mid Atlantic Retina, Philadelphia (YY).

Poster presented at the Retina Society Meeting in October 2017 in Boston.

Dr. Shizuo Mukai is supported in part by gifts to the Mukai Fund and the Massachusetts Eye and Ear Infirmary, Boston. The remaining authors report no relevant financial disclosures.

Address correspondence to Michael P. Blair, MD, 2454 E Dempster St., Suite 400, Des Plaines, IL, 60016; email: michaelblairmd@gmail.com.

Received: August 25, 2018
Accepted: March 22, 2019

10.3928/23258160-20191031-12

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