Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Comparison Between Ultra-Widefield Pseudocolor Imaging and Indirect Ophthalmoscopy in the Detection of Peripheral Retinal Lesions

Giovanni Fogliato, MD; Enrico Borrelli, MD; Lorenzo Iuliano, MD; Andrea Ramoni, MD; Lea Querques, MD; Alessandro Rabiolo, MD; Francesco Bandello, MD, FEBO; Giuseppe Querques, MD, PhD

Abstract

BACKGROUND AND OBJECTIVE:

To systematically compare the intermodality and inter-rater agreement for indirect ophthalmoscopy and ultra-widefield (UWF) imaging in detecting peripheral retinal lesions predisposing to retinal rhegmatogenous detachment.

PATIENTS AND METHODS:

In this prospective, observational, cross-sectional study, patients with a previous diagnosis of peripheral retinal lesions were enrolled. UWF pseudocolor imaging and dilated fundus examination were obtained.

RESULTS:

Thirty-seven eyes (20 patients, 12 females) were enrolled. The level of inter-rater agreement was excellent in both the ophthalmoscopy-based and UWF-based assessment. The overall agreement in the UWF-based assessment was found to be Kappa = 0.874 (P < .0001). The UWF-based evaluation was demonstrated to have a sensitivity of 89.2% in detecting peripheral retinal lesions. In the sectorial analysis, the UWF-based reading had a lower sensitivity in the inferior sector.

CONCLUSION:

The identification of peripheral retinal lesions with UWF imaging allowed for an accurate and reproducible assessment.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:544–549.]

Abstract

BACKGROUND AND OBJECTIVE:

To systematically compare the intermodality and inter-rater agreement for indirect ophthalmoscopy and ultra-widefield (UWF) imaging in detecting peripheral retinal lesions predisposing to retinal rhegmatogenous detachment.

PATIENTS AND METHODS:

In this prospective, observational, cross-sectional study, patients with a previous diagnosis of peripheral retinal lesions were enrolled. UWF pseudocolor imaging and dilated fundus examination were obtained.

RESULTS:

Thirty-seven eyes (20 patients, 12 females) were enrolled. The level of inter-rater agreement was excellent in both the ophthalmoscopy-based and UWF-based assessment. The overall agreement in the UWF-based assessment was found to be Kappa = 0.874 (P < .0001). The UWF-based evaluation was demonstrated to have a sensitivity of 89.2% in detecting peripheral retinal lesions. In the sectorial analysis, the UWF-based reading had a lower sensitivity in the inferior sector.

CONCLUSION:

The identification of peripheral retinal lesions with UWF imaging allowed for an accurate and reproducible assessment.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:544–549.]

Introduction

Peripheral retinal degenerations are common alterations that may predispose eyes to rhegmatogenous retinal detachment (RRD). These lesions vary in prevalence and rate of progression to RRD, as well as in clinical characteristics.1 Furthermore, these lesions may coexist. As an example, retinal tears are found in 1.4% of eyes affected by lattice degeneration.2

Patients with peripheral retinal pathology may experience various symptoms, including floaters and phosphenes. However, since such symptoms have low specificity, the clinical assessment remains the gold standard for the diagnosis and follow-up of these lesions. This requires a thorough evaluation, incorporating a detailed patient history and a stereoscopic examination of the entire retina through a dilated pupil. In addition, the evaluation of conditions predisposing eyes to retinal detachment requires knowledge of peripheral vitreoretinal diseases that may predispose to detachment. However, the diagnosis may be difficult given the unenforceable mydriasis and low compliance in a number of patients, as well as the lack of retinal specialists in some primary eye care institutions.

Ultra-widefield (UWF) imaging has become a key tool in the clinical care of patients with various retinal disorders. The California device (Optos, Dunfermline, Scotland) is a confocal scanning laser ophthalmoscope-based system that uses an ellipsoidal mirror to obtain a wide (up to 200°) visualization of the retina. This system provides a pseudocolor (two-color) image of the retina using red and green laser wavelengths to illuminate the retina. The green (red-free) component of the resulting image depicts the retina and its vasculature, whereas the red component highlights deeper structures.3 Important advantages of this imaging system include fast imaging speed without the necessity of pupil dilation, high resolution, and the capability to enhance the obtained images before these being reviewed.3

Given the need of community-based care for a reproducible, fast, comfortable, and easily interpretable tool in investigating patients with retinal symptoms, this study was designed to systematically compare the inter-rater agreement for UWF images and dilated fundus examination in detecting peripheral retinal lesions predisposing to RRD, including retinal tear, retinal hole, lattice degeneration, and snail track degeneration. Importantly, we investigated the sensitivity of UWF pseudocolor imaging as a screening tool for the detection of peripheral retinal pathology.

Patients and Methods

Study Participants

This study is a prospective, observational, cross-sectional case series. Patients with a previous clinical confirmed diagnosis of peripheral retinal lesions were enrolled from the Medical Retina & Imaging Unit and the Vitreo-Retinal Unit at the San Raffaele Hospital in Milan, Italy. The study was approved by the institutional review board and adhered to the tenets of the Declaration of Helsinki. Written informed consent was obtained from all subjects prior to enrollment in the study.

All patients were enrolled between January 2016 and June 2017 and received a complete ophthalmologic examination. Two retinal specialists (AR and GF, observer-1 and observer-2, respectively) independently performed slit-lamp biomicroscopy and dilated fundus examination.

To be included, patients were required to have history of peripheral retinal pathology, including presence of retinal tear, retinal hole, lattice degeneration, and snail track degeneration. Patients with insufficiently clear media to allow retinal imaging or inability to obtain images of sufficient quality to be graded were excluded.

Imaging and Grading Protocol

All imaging was performed before pupillary dilation. The ultra-widefield imaging was performed using the Optos California device. This system uses two laser wavelengths to illuminate the retina, set at 532 nm (green laser) and 635 nm (red laser), respectively. Using these two wavelengths, this device provides a pseudocolor (two-color) image in less than 0.4 seconds.

Pseudocolor images were obtained by a trained physician, as previously described.4,5 In brief, subjects were seated in front of the Optos device and instructed to look at a green fixation target. Once the correct position and focus was achieved, the examiner was able to press a button to capture the image. The image could be immediately viewed by the examiner and repeated if necessary. Each patient had several images obtained for each of the gaze position (ahead, superior, inferior, right, left). The best for quality were thus included in the grading process.

Two experienced graders (GQ and LQ, reader-1 and reader-2, respectively) independently graded the UWF pseudocolor images for the presence of peripheral retinal lesions (Figures 1 and 2). The images were examined using the built-in software which allows images to be magnified, as well as several variables (eg, contrast and brightness) to be adjusted.

Pseudocolor image from the left eye of a patient affected by a retinal tear located in the superior peripheral retina.

Figure 1.

Pseudocolor image from the left eye of a patient affected by a retinal tear located in the superior peripheral retina.

Pseudocolor image from the right eye of a patient affected by lattice degeneration located in the inferior peripheral retina.

Figure 2.

Pseudocolor image from the right eye of a patient affected by lattice degeneration located in the inferior peripheral retina.

The presence and position (inferior, temporal, superior, and nasal sectors) of any investigated lesions were noted by both observers and graders.

After grading and clinical assessment of all the cases was completed, a single graded image (reader-1) and clinical evaluation (observer-1) were selected for each case to calculate the UWF imaging sensitivity.

Statistical Analysis

Statistical calculations were performed using Statistical Package for Social Sciences (version 20.0; SPSS, Chicago, IL).

For each modality of assessment (UWF pseudocolor imaging and indirect ophthalmoscopy) the kappa statistic was determined to investigate the inter-rater agreement. Sensitivity for detection of peripheral retinal lesions using the UWF images was calculated as the number of eyes with lesions identified on UWF pseudocolor evaluation (numerator) divided by the number of eyes with lesions identified with the gold standard examination (indirect ophthalmoscopy – denominator). The chosen level of statistical significance was a P value of less than .05.

Results

Thirty-seven eyes (20 patients, 12 females) with peripheral retinal lesions were enrolled. Mean age of the patients enrolled was 46.0 years ± 16.5 years (range: 20 years to 74 years).

Of the 37 cases included in the analysis, the UWF-based grading identified peripheral lesions in 33 (reader-1) and 32 (reader-2) eyes. The overall characteristics of lesions identified by observers and readers are shown in the Table 1.

Characteristics of Lesions Identified by Observers and Readers

Table 1:

Characteristics of Lesions Identified by Observers and Readers

Inter-Rater Agreement

The level of inter-rater agreement was excellent, in both the ophthalmoscopy-based (between the two observers) and UWF-based (between the two readers) assessments, respectively (Table 2). The overall agreement in the UWF-based assessment was found to be Kappa = 0.874 (P < .0001). In the sectorial analysis, the lowest agreement was in the inferior sector, in both the UWF-based (Kappa = 0.937; P < .0001) and indirect ophthalmoscopy-based (Kappa = 0.891; P < .0001) assessments (Table 2). The identification of lattice degeneration showed the lowest agreement between observers (Kappa = 0.877; P < .0001) and readers (Kappa = 0.934; P < .0001).

Results of Inter-Rater Agreement and Ultra-Widefield Sensitivity

Table 2:

Results of Inter-Rater Agreement and Ultra-Widefield Sensitivity

Ultra-Widefield Sensitivity

Table 2 summarizes the sensitivity of the UWF-based assessment for the identification of peripheral lesions. Overall, this assessment was demonstrated to have a sensitivity of 89.2%, as compared to the gold standard indirect ophthalmoscopy-based evaluation.

In the sectorial analysis, the UWF-based reading granted a detection of 20 out of 22 lesions in the superior sector (sensitivity of 90.9%), 20 out of 20 lesions in the temporal sector (sensitivity of 100.0%), 20 out of 26 lesions in the inferior sector (sensitivity of 76.9%), and three out of three lesions in the nasal sector (sensitivity of 100.0%) (Table 2).

In the UWF-based assessment, seven out of eight retinal tears (sensitivity = 87.5%), seven out of eight retinal holes (sensitivity = 87.5%), 11 out of 12 lattice degenerations (sensitivity = 91.7%), and 21 out of 25 snail track degenerations (sensitivity of 84.0%) were identified (Table 2).

Discussion

In this prospective, cross-sectional study, we investigated the usefulness of UWF pseudocolor images in the detection of peripheral retinal lesions. Overall, we did observe that the assessment of UWF pseudocolor images allowed for an accurate and reproducible identification of peripheral retinal pathology, as compared with conventional dilated fundus examination. Because the purpose of our study was to investigate the sensitivity and reproducibility of UWF-based grading in the detection of retinal lesions predisposing to RRD (retinal tear, retinal hole, lattice degeneration, and snail track degeneration), we did not assess for the presence of other lesions.

The use of UWF imaging has been demonstrated to be valuable in the diagnosis and treatment of several ocular disorders, including retinal vascular diseases, retinal and choroidal dystrophies, and retinal inflammatory disorders.3,6–8 Importantly, UWF images have been proposed as an useful adjunct to the clinical examination for characterizing eyes with retinal detachments.9 Witmer et al.9 reported on 16 cases of acute, nontraumatic RRD imaged with UWF pseudocolor and autofluorescence. The authors demonstrated that the large depth-of-field allows for an accurate delineation of the RRD size and a high sensitivity in detecting the causative retinal breaks. In addition, UWF imaging provides an efficient way for the vitreoretinal surgeon to record the outcomes of surgical interventions, given the images may be obtained even in the presence of a gas bubble and can be ultimately used to monitor the extent, absorption, and recurrence of subretinal fluid.10

Although UWF imaging has been demonstrated to be useful in the characterization of eyes with retinal detachment, previous reports have shown that this imaging modality has a lower sensitivity in the detection of peripheral retinal lesions without RRD in comparison with indirect ophthalmoscopy.4,5 In a study of 60 patients with peripheral retinal pathology, UWF imaging was compared to indirect ophthalmoscopy for detecting retinal peripheral lesions.4 In this study, two masked readers evaluated the images independently and identified possible retinal lesions requiring referral to a retinal specialist. The UWF sensitivity was demonstrated to be low to moderate (74%), especially for lesions anterior to the equator.4 In a more recent study, Khandhadia et al.5 included 205 eyes of 187 patients with retinal symptoms (flashing lights and floaters) and compared the findings from UWF images and casualty officer with a gold-standard examination with indirect ophthalmoscopy performed by a retinal specialist. The sensitivity to detect retinal holes/tears (n=18) was 33% and 67% for the UWF imaging review and the casualty officers' evaluation, respectively.

In contrast, our results showed that UWF pseudocolor images have a high sensitivity in detecting retinal peripheral lesions. The disagreement with previous reports might be secondary to the technical advances that have occurred in the last years and were implemented in the device we used for this study. One of the main limitations of the preceding UWF devices was the peripheral distortion resulting in a difficult assessment of this retinal periphery.11,12 This distortion is intrinsic to the UWF device and is due to the ellipsoidal mirror used to obtain a broad viewing angle causing a magnification of the peripheral retina, which looks artifactually stretched. However, recent advances in software algorithms have overcome this limitation using a stereographic projection software that maintains the same angular relationship at every eccentricity.13 Furthermore, an increased image resolution (lateral resolution of 10 μm in the device used for this study) and contrast sensitivity has further improved our capability to assess the peripheral retina.3

Importantly, our data demonstrated a lower sensitivity in the superior and inferior fields, whose assessment may be challenging due to artifacts that may confound their visualization, given that the very large depth-of-focus commonly results in the patient's eyelashes to appear in the image.14

Notably, our results showed an excellent inter-rater agreement in the UWF-based assessment of the peripheral retina. Taken together, these results do suggest that UWF imaging may become a useful tool in the assessment of eyes with lesions of the peripheral retina, with a high sensitivity and reproducibility. Even though we did not include a control group of normal eyes to investigate the specificity of the UWF-based assessment, our study may increase the acceptance for this technique as imaging tool in the community-based retinal assessment of patients experiencing retinal symptoms (eg, floaters and flashing lights).

Our study has some limitations that should be considered when assessing our findings. First, the sample size of the cohort is relatively small, which reduces the power of our analysis. Second, our patients were imaged and graded by expert technician and graders, respectively. This aspect may have caused the potential for research bias. Therefore, adequate training for high-quality image acquisition and interpretation is essential to reproduce our results. Finally, as explained above, we did enroll patients with clinically diagnosed presence of peripheral retinal lesions. For this reason, our observations are limited in that we are not able to assess the specificity of this assessment.

In summary, using UWF pseudocolor imaging allowed an accurate and reproducible identification of lesions in the peripheral retina. If these results are validated in further studies, this imaging technique may emerge as an essential tool to explore the retina of patients experiencing retinal symptoms.

References

  1. Lewis H. Peripheral retinal degenerations and the risk of retinal detachment. Am J Ophthalmol. 2003;136(1):155–160. doi:10.1016/S0002-9394(03)00144-2 [CrossRef]12834683
  2. Straatsma B, Zeegan P, Foos R, Feman S, Shabo A. Edward Jackson Memorial Lecture. Lattice degeneration of the retina. Trans Am Acad Ophthalmol Otolaryngol. 1974;78(2):87–113.
  3. Nagiel A, Lalane RA, Sadda SR, Schwartz SD. Ultra-widefield fundus imaging. Retina. 2016;36(4):660–678. doi:10.1097/IAE.0000000000000937 [CrossRef]27014860
  4. Mackenzie PJ, Russell M, Ma PE, Isbister CM, Maberley DAL. Sensitivity and specificity of the Optos Optomap for detecting peripheral retinal lesions. Retina. 2007;27(8):1119–1124. doi:10.1097/IAE.0b013e3180592b5c [CrossRef]18040256
  5. Khandhadia S, Madhusudhana KC, Kostakou A, Forrester JV, Newsom RS. Use of Optomap for retinal screening within an eye casualty setting. Br J Ophthalmol. 2009;93(1):52–55. doi:10.1136/bjo.2008.148072 [CrossRef]
  6. Fan W, Uji A, Borrelli E, et al. Precise measurement of retinal vascular bed area and density on ultra-wide fluorescein angiography in normal subjects. Am J Ophthalmol. 2018;188:155–163. doi:10.1016/j.ajo.2018.01.036 [CrossRef]29428456
  7. Rabiolo A, Marchese A, Sacconi R, et al. Refining Coats' disease by ultra-widefield imaging and optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol. 2017;255(10):1881–1890. doi:10.1007/s00417-017-3794-7 [CrossRef]28875282
  8. Marchese A, Rabiolo A, Corbelli E, et al. Ultra-widefield imaging in patients with angioid streaks secondary to pseudoxanthoma elasticum. Ophthalmol Retin. 2017;1(2):137–144. doi:10.1016/j.oret.2016.10.005 [CrossRef]
  9. Witmer MT, Cho M, Favarone G, Chan RVP, D'Amico DJ, Kiss S. Ultra-wide-field autofluorescence imaging in non-traumatic rhegmatogenous retinal detachment. Eye (Lond). 2012;26(9):1209–1216. doi:10.1038/eye.2012.122 [CrossRef]
  10. Anderson L, Friberg TR, Singh J. Ultrawide-angle retinal imaging and retinal detachment. Semin Ophthalmol. 2007;22(1):43–47. doi:10.1080/08820530601162867 [CrossRef]17366119
  11. Oishi A, Hidaka J, Yoshimura N. Quantification of the Image obtained with a wide-field scanning ophthalmoscope. Invest Opthalmology Vis Sci. 2014;55(4):2424. doi:10.1167/iovs.13-13738 [CrossRef]
  12. Croft DE, van Hemert J, Wykoff CC, et al. Precise montaging and metric quantification of retinal surface area from ultra-widefield fundus photography and fluorescein angiography. Ophthalmic Surg Lasers Imaging Retina. 2014;45(4):312–317. doi:10.3928/23258160-20140709-07 [CrossRef]25037013
  13. Sagong M, van Hemert J, Olmos de Koo LC, Barnett C, Sadda SR. Assessment of accuracy and precision of quantification of ultra-widefield images. Ophthalmology. 2015;122(4):864–866. doi:10.1016/j.ophtha.2014.11.016 [CrossRef]25576995
  14. Inoue M, Yanagawa A, Yamane S, Arakawa A, Kawai Y, Kadonosono K. Wide-field fundus imaging using the Optos Optomap and a disposable eyelid speculum. JAMA Ophthalmol. 2013;131(2):226–227. doi:10.1001/jamaophthalmol.2013.750 [CrossRef]23411888

Characteristics of Lesions Identified by Observers and Readers

Indirect OphthalmoscopyUltra-Widefield Imaging


Obersver-1Observer-2Reader-1Reader-2

No. of Eyes With Identified Lesions
  Whole periphery, n37373332
  Superior, n22222019
  Temporal, n20202020
  Inferior, n26252020
  Nasal, n3333

Type of Lesion Identified
  Retinal tear, n8877
  Retinal hole, n8877
  Lattice degeneration, n12121110
  Snail track degeneration, n25252120

Results of Inter-Rater Agreement and Ultra-Widefield Sensitivity

Inter-Rater AgreementUltra-Widefield Imaging Sensitivity

Indirect OphthalmoscopyUltra-Widefield Imaging

Identification of Lesions
  Whole periphery0.874 (P< .0001)89.2%
  Superior1.0 (P < .0001)0.946 (P < .0001)90.9%
  Temporal1.0 (P < .0001)1.0 (P < .0001)100.0%
  Inferior0.937 (P < .0001)0.891 (P < .0001)76.9%
  Nasal1.0 (P < .0001)1.0 (P < .0001)100.0%

Type of Lesion Identified
  Retinal tear1.0 (P < .0001)1.0 (P < .0001)87.5%
  Retinal hole1.0 (P < .0001)1.0 (P < .0001)87.5%
  Lattice degeneration0.877 (P < .0001)0.934 (P < .0001)91.7%
  Snail track degeneration1.0 (P < .0001)0.945 (P < .0001)84.0%
Authors

From the Department of Ophthalmology, Ospedale San Raffaele Scientific Institute, University Vita-Salute, Milan (GF, EB, LI, AR, LQ, AR, FB, GQ); and Ophthalmology Clinic, Department of Medicine and Science of Ageing, University G. D'Annunzio Chieti-Pescara, Chieti, Italy (EB).

Dr. G. Querques is a speaker for Allergan, Alimera, Amgen, Bayer, KHB, Novartis, Roche, Sandoz, and Zeiss, as well as a consultant to Allergan, Alimera, Bausch + Lomb, Bayer, Heidelberg Engineering, Novartis, and Zeiss. Dr. Bandello is a speaker for Allergan, Alimera, Bayer, Farmila-Thea, Schering Pharma, Sanofi-Aventis, Novagali, Pharma, Hoffmann-La Roche, Genentech, and Novartis. The remaining authors report no relevant financial disclosures.

Drs. Fogliato and Borrelli equally contributed to this paper and should be considered as co-first authors.

Address correspondence to Giuseppe Querques, MD, PhD, Department of Ophthalmology, University Vita-Salute San Raffaele, Via Olgettina 60, Milan, Italy; email: giuseppe.querques@hotmail.it.

Received: August 21, 2018
Accepted: January 17, 2019

10.3928/23258160-20190905-02

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