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International Journal of Retina and Vitreous logoLink to International Journal of Retina and Vitreous
. 2020 Aug 3;6:35. doi: 10.1186/s40942-020-00237-w

Reliability of foveal avascular zone measurements in eyes with retinal vein occlusion using optical coherence tomography angiography

Bruno Mauricio Rodrigues de Oliveira 1,, Luis Filipe Nakayama 1, Bruno Rebello de Godoy 1, Alexandre Gomes Bortoloti de Azevedo 1, Flavio Eduardo Hirai 1, Somaia Mitne 1
PMCID: PMC7398327  PMID: 32774887

Abstract

Background

To evaluate the reliability of foveal avascular zone (FAZ) area measurements using optical coherence tomography angiography (OCTA) in eyes with retinal vein occlusion (RVO).

Methods

Twenty-five OCTA exams of patients with RVO were evaluated retrospectively. Three examiners performed manual measurements of the FAZ, and interrater and intrarater reliability were obtained.

Results

The intraclass correlation coefficient (ICC) for interrater reliability for individual measurements was 0.62 (moderate) with a 95% confidence interval (CI) of 0.40 to 0.79 (p < 0.001). The ICC (95% CI) for intrarater reliability was 0.92 (0.82 to 0.96) for rater A, 0.96 (0.91 to 0.98) for B, and 0.88 (0.76 to 0.94) for C (p < 0.001). In all subanalyses including presence of edema and type of occlusion, interrater reliability was poor/moderate, and intrarater reliability was good/excellent.

Conclusion

The FAZ varies significantly among eyes with RVO, so measurements obtained using OCTA should be analyzed with caution due to the moderate level of reliability among different examiners.

Keywords: Retina, Foveal avascular zone, OCT, Retinal vein occlusion

Background

Retinal vein occlusion (RVO) is a common retinal vascular disease that may lead to significant visual morbidity. The vascular obstruction can occur either in the central retinal vein or in a branch of the retinal vein [13]. Systemic vascular diseases are the most important risk factor for RVO, especially in elderly patients. Hypercoagulable states and systemic inflammatory conditions are also risk factors that must be considered in young patients, in whom RVO is uncommon.

Visual outcome depends on the severity of retinal ischemia and macular edema. Hence, evaluation of the retinal vasculature is important for determining the therapeutic strategy and prognosis [13].

Fluorescein angiography (FA) has traditionally been used to analyze retinal capillary non-perfusion and neovascularization. FA is an invasive procedure involving intravenous dye injection that provides two-dimensional images with dynamic visualization of blood flow. Therefore, patterns of leakage, pooling and staining can be observed and correlated with clinical presentation. However, FA is unable to analyze the different retinal vasculature layers separately [4, 5].

The optical coherence tomography angiography (OCTA) allows visualization of vascular maps of the retina and choroid separated by layers and non-invasively [6, 7]. OCTA can provide structural and functional information on the retina and choroidal vascularization and detect vascular flow at a fixed point in time [6]. In addition, due to the high resolution of the capillary information, OCTA permits measurement of the dimensions of the foveal avascular zone (FAZ). Previous studies have demonstrated the reliability of FAZ measurements by OCTA compared with the contralateral eye, albeit with great interobserver variability [810]. However, software platforms lack normalized data to determine whether microvascular changes are abnormal, and the reliability of FAZ measurements using OCTA in vascular retinal diseases is unclear [11, 12].

The aim of this study was to evaluate the reliability of FAZ area measurements in eyes with RVO obtained by swept-source OCTA using a Topcon DRI OCT Triton.

Methods

OCTA exams of consecutive patients attending retinal clinics at Federal University of São Paulo and diagnosed with RVO in the last 2 years were analyzed retrospectively. This study was approved by the UNIFESP Institutional Review Board and carried out in accordance with the tenets of the Declaration of Helsinki (Additional file 1).

The inclusion criteria were diagnosis of RVO (central or branch of the retinal vein) according to clinical evaluation and fundus retinal exam performed by at least two retina specialists. Patients were excluded from this study if their medical records documented a history of another ocular or clinical disease that may lead to retinal vascular abnormalities.

A Topcon DRI Triton swept-source optical coherence tomographer (Topcon Corporation, Japan) was used to obtain volumetric angiography maps of the retina. All exams met the quality thresholds given by the OCT software with a minimum index of 40. A macular scan size of 6 × 6 mm was used for FAZ evaluation at the superficial retinal vascular layer. Manual measurements were performed using the built-in IMAGEnet® software (Topcon Medical Systems, Inc.). Two retina specialists and one-third-year ophthalmology resident were recruited to perform the measurements of all patients blinded to each other’s results.

Every examiner performed two measurements of each image at different times with an interval of at least 3 weeks between the two measurements. Before measurement, evaluation and correction of the segmentation of retinal layers for angiography analysis were performed at the discretion of the examiner. A previous study reported the importance of adjusting segmentation, including the full thickness of the retina, in order to reduce errors and variations [13].

Statistical analysis was performed with Stata v.14 (College Station, Texas, USA). To evaluate the interrater (between-observer) reliability of the measurements, we calculated the intraclass correlation coefficient (ICC) using a two-way random-effects model evaluating single raters for absolute agreement. For the intrarater (within-observer) reliability test, we used a two-way mixed-effects model for absolute agreement between measurements within the rater.

The ICC takes a value from zero (no agreement) to one (complete agreement). For analysis purposes, we classified ICC values as follows: 0 to 0.50, poor reliability; 0.50 to 75, moderate reliability; 0.75 to 0.90, good reliability; and greater than 0.90, excellent reliability.

Results

Twenty-five patients were enrolled in this study, including 14 (56%) males and 11 (44%) females. The diagnosis was central RVO in 14 patients (56%) and branch RVO in 11 patients (44%). Eighteen patients (72%) presented OCT scans with macular edema. The mean age of the patients was 56.7 (SD 12.5) years, with a range from 30 to 78 years (Table 1).

Table 1.

Baseline characteristics of patients

Characteristics Sample (total = 25)
Gender
 Male 14 (56%)
 Female 11 (44%)
Type of occlusion
 Central vein 14 (56%)
 Branch vein 11 (44%)
Mean age (SD) 56.7 (12.5)
Presence of macular edema 18 (72%)
Affected eye
 Right eye 11 (44%)
 Left eye 14 (56%)

The individual FAZ measurements of the patients are shown in Table 2, along with the mean FAZ dimensions provided by each examiner (A, B and C). To evaluate the consistency of the measurement process, statistical analysis was performed using the ICC to determine the repeatability (intrarater reliability) and reproducibility (interrater reliability).

Table 2.

Foveal avascular zone (FAZ) measurements of each examiner

FAZ A1 FAZ A2 Mean A FAZ B1 FAZ B2 Mean B FAZ C1 FAZ C2 Mean C
1 529.453 519.609 524.531 986.836 1094.766 1040.801 862.646 835.313 848.9795
2 312.539 361.758 337.1485 355.078 285.5 320.289 359.297 451.406 405.3515
3 665.859 848.32 757.0895 351.563 375.117 363.34 316.758 412.734 364.746
4 529.805 502.031 515.918 531.211 525.586 528.3985 567.07 576.211 571.6405
5 880.312 582.188 731.25 504.492 547.031 525.7615 519.258 512.578 515.918
6 545.625 926.367 735.996 411.328 525.234 468.281 672.891 1050.82 861.8555
7 959.766 941.484 950.625 724.219 687.305 705.762 685.195 680.625 682.91
8 392.695 273.516 333.1055 1174.219 1086.68 1130.4495 1406.602 1087.734 1247.168
9 627.188 387.422 507.305 423.984 421.523 422.7535 413.086 387.07 400.078
10 338.203 289.336 313.7695 443.32 368.789 406.0545 365.625 358.242 361.9335
11 696.797 685.195 690.996 421.875 837.773 629.824 1147.5 770.273 958.8865
12 413.086 533.32 473.203 354.375 348.398 351.3865 288.281 241.172 264.7265
13 1506.797 1195.313 1351.055 773.438 1213.594 993.516 929.531 1499.063 1214.297
14 1376.719 1406.953 1391.836 1429.102 1595.742 1512.422 1495.47 1514.18 1504.825
15 206.719 265.43 236.0745 63.281 72.422 67.8515 80.156 85.43 82.793
16 844.102 731.602 787.852 684.492 688.008 686.25 622.969 427.5 525.2345
17 566.367 492.188 529.2775 601.172 759.375 680.2735 390.586 385.684 388.135
18 1523.672 1567.07 1545.371 1978.945 2036.602 2007.7735 366.328 309.727 338.0275
19 661.641 648.984 655.3125 224.648 208.125 216.3865 184.922 145.625 165.2735
20 706.992 736.523 721.7575 355.586 364.57 360.078 342.773 248.203 295.488
21 145.195 192.656 168.9255 76.641 74.883 75.762 218.32 235 226.66
22 265.078 315 290.039 229.57 239.06 234.315 140.977 146.25 143.6135
23 356.836 359.648 358.242 318.516 312.188 315.352 253.447 262.969 258.208
24 368.086 458.086 413.086 485.156 464.063 474.6095 317.461 348.398 332.9295
25 418.359 557.227 487.793 75.937 93.164 84.5505 396.211 354.375 375.293

The ICC for interrater reliability for individual measurements was 0.62 (moderate), with a 95% confidence interval (CI) of 0.40 to 0.79 (p < 0.001). When considering all raters as a group and analyzing the reliability between the average measurements, the ICC value was 0.83 (good), with a 95% CI of 0.67 to 0.92 (p < 0.001).

The ICC (95% CI) for intrarater reliability was 0.92 (0.82 to 0.96) for rater A, 0.96 (0.91 to 0.98) for rater B, and 0.88 (0.76 to 0.94) for rater C; these differences were significant (p < 0.001).

Considering macular edema and type of occlusion (central or branch RVO), the ICC for interrater reliability for individual measurements was 0.75 (moderate) for central RVO (95% CI 0.51–0.90 and p < 0.001); 0.48 (poor) for branch RVO (95% CI 0.12–0.80 and p < 0.05); 0.62 (moderate) for macular edema (95% CI 0.36–0.82 and p < 0.001); and 0.58 (moderate) for the group without macular edema (95% CI 0.11–0.90 and p < 0.05).

For the above subanalyses, the intrarater reliabilities of raters A, B and C were all good/excellent with statistical significance (p < 0.001), as shown in Table 3. There was no difference in reliability comparing different types of occlusion or presence of edema in the intrarater analysis.

Table 3.

Intraclass correlation coefficient (ICC) for reliability analysis of foveal avascular zone (FAZ) measurements

Rating ICC 95% conf. interval
Interrater reliability
 Individual 0.62 0.41 0.79
 Average 0.83 0.67 0.92
Intrarater reliability
 A 0.92 0.82 0.96
 B 0.96 0.91 0.98
 C 0.88 0.76 0.94
Interrater reliability—type of occlusion
 Central vein occlusion*
  Individual 0.75 0.51 0.90
  Average 0.90 0.76 0.96
 Branch vein occlusion**
  Individual 0.48 0.12 0.80
  Average 0.74 0.29 0.92
Interrater reliability—presence of edema
 Macular edema
  Individual 0.62 0.36 0.82
  Average 0.83 0.63 0.93
 Without macular edema
  Individual 0.58 0.11 0.90
  Average 0.81 0.28 0.96
Intrarater reliability—type of occlusion
 Central vein occlusion
  A 0.91 0.75 0.97
  B 0.99 0.96 0.99
  C 0.94 0.81 0.98
 Branch vein occlusion
  A 0.93 0.75 0.98
  B 0.94 0.80 0.98
  C 0.79 0.40 0.94
Intrarater reliability—presence of edema
 Macular edema
  A 0.91 0.78 0.97
  B 0.93 0.83 0.97
  C 0.87 0.69 0.95
 Without macular edema
  A 0.91 0.57 0.98
  B 0.98 0.87 0.99
  C 0.90 0.53 0.98

p < 0.001, *p < 0.001, **p < 0.05

Discussion

The FAZ is the macular capillary-free zone surrounded by interconnected capillary vessels. Its size correlates with the foveal circulation condition in retino-vascular diseases [13]. Previous studies have suggested a mean physiological FAZ area of 200 to 400 μm2 in healthy subjects [8]. RVO leads to FAZ enlargement, and measurements of the FAZ therefore provide an objective evaluation of macular ischemia and consequently visual acuity prognosis [1].

Fluorescein angiography (FA) is the standard exam for FAZ evaluation, but the high variability in measurements diminishes the reliability of this method, even in healthy patients [8]. FA may also miss some microvasculature changes that are more readily observed in OCTA, including deep capillary plexus, which is mainly affected in RVO [1, 11]. Moreover, the FA exam cannot be performed in pregnant women and patients with fluorescein allergy, renal failure, severe asthma or significant cardiac disease [5].

OCTA is a dye-less method of imaging retinal circulation in different layers that allows a volumetric approach.

To avoid segmentation artifact manual correction of automatic retinal layers segmentation were performed in all OCT exams. En face retinal exam were evaluated to identify hemorrhages or opacities that could lead to shadowing and projection artifacts. In every OCTA exam artifacts must be considered and manual correction should be performed to decrease artifacts in exam and en face exam need to be analyzed altogether with OCTA vascular exam to reduce shadowing and projections artifacts.

Previous OCTA studies in healthy patients have suggested excellent reproducibility and repeatability in measurements of the FAZ [8], but few studies have considered macular pathologies such as macular ischemia or edema [14]. Although several studies have aimed to correlate OCTA findings such as enlargement of FAZ area, vascular network attenuation and retinal nonperfusion with the severity of retinal vascular diseases [2, 1519], the reasons for the large variability in prognosis among patients and the role and impact of such anatomic features in clinical outcomes remain unclear [2]. Previous reports have identified qualitative and quantitative changes associated with RVO via OCTA. However, whether the quantitative data provided by OCTA software are accurate and can be correlated with macular function have not been established [11].

The present report indicated good/excellent intrarater reliability of manual FAZ measurements and satisfactory repeatability of FAZ area measurements via OCTA. By contrast, interrater reliability (i.e., reproducibility) was moderate, suggesting that FAZ measurements by different observers may not be comparable. Moreover, the great variability of FAZ dimensions (as shown in Table 2 and Fig. 1) make correlations with disease severity difficult. In addition, the present study did not demonstrate whether the type of occlusion and the presence of macular edema are factors that impact the reliability of FAZ measurements, even after review and correction of the segmentation of retinal layers for angiography analysis.

Fig. 1.

Fig. 1

OCTA maps of three different subjects with great variability of foveal avascular zone

The main concern about OCTA image interpretation is the presence of artifacts, specially segmentation, projection, and masking artifacts. As mentioned above, segmentation artifacts can be reduced by using manual correction of retinal layers. Also, evaluation of en face retinal maps could avoid projection artifacts misinterpretation. However, a pronounced edema or highly reflective intraretinal structures could produce masking artifacts in underlying layers [20]. Previous reports noticed the absence of capillaries detection in the areas of retinal cysts [21, 22]. Couturier et al. hypothesized that retinal cysts provoke a displacement of the capillary in the cysts edges or more likely the cysts develop preferentially in nonperfusion areas [21]. Sellam et la reported that after cyst regression only 36% of the eyes improved vascular density in these areas [22].

The large number of artifacts in OCTA images segmentation and masking effects may complicate the proper judgement of FAZ limits, resulting in an irregular and inaccurate vascular map close to the fovea. Consequently, the results may not be interchangeable among patients. However, the good intrarater reliability observed in the present study suggests that the use of FAZ measurements for individual follow-up is feasible.

Conclusion

In summary, caution is advised when analyzing measurements of the FAZ area in eyes with RVO. Comparisons between examiners provide only moderate reliability, and the results may not be interchangeable.

Supplementary information

40942_2020_237_MOESM1_ESM.pdf (35.7KB, pdf)

Additional file 1. Ethics Committee Approval provided by UNIFESP Institutional Review Board.

Acknowledgements

We would like to thank Ophthalmology sectors from Escola Paulista de Medicina/São Paulo Federal University.

Authors’ contributions

BRG, AGBA and BMRO conceived and planned the manuscript. LFN and BMRO took the lead in writing and reviewing the manuscript. All authors contributed in an extensive exchange. SM coordinated the research. All authors read and approved the final manuscript.

Funding

No funding

Availability of data and materials

The datasets generated during the current study that were used to calculate the primary outcome parameters are available upon reasonable request from the corresponding author Oliveira, BMR.

Ethics approval and consent ot participate

Ethic Committee Number Unifesp: 0492/2019; CAAE: 12801919.3.0000.5505. All participants signed informed consent.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Bruno Mauricio Rodrigues de Oliveira, Email: brunomro@gmail.com.

Luis Filipe Nakayama, Email: nakayama.luis@gmail.com.

Bruno Rebello de Godoy, Email: br.rgodoy@gmail.com.

Alexandre Gomes Bortoloti de Azevedo, Email: alexandregbazevedo@gmail.com.

Flavio Eduardo Hirai, Email: fhirai@yahoo.com.

Somaia Mitne, Email: somitne@gmail.com.

Supplementary information

Supplementary information accompanies this paper at 10.1186/s40942-020-00237-w.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

40942_2020_237_MOESM1_ESM.pdf (35.7KB, pdf)

Additional file 1. Ethics Committee Approval provided by UNIFESP Institutional Review Board.

Data Availability Statement

The datasets generated during the current study that were used to calculate the primary outcome parameters are available upon reasonable request from the corresponding author Oliveira, BMR.


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