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Dr. Romit Salian, S17177, Dr. Narendran V, Dr. Karan A.K., Dr. Saravanan V R

ABSTRACT:

Aim:

To study and assess the role of OCT- Angiography, in detecting changes in foveal avascular zone characteristics in eyes with diabetic macular edema and to compare these characteristics with gold standard fundus fluorescence angiography.

Methods:

A cross sectional observational study conducted in our hospital from may 2016 to may 2017. 38 eyes of 21 patients with diabetic macular edema was included in the study. Each of these patients underwent comprehensive ocular and systemic evaluation. The data was compiled aftercomparing the Foveal Avascular Zone characteristics in Optical Coherence Topography-Angiography(OCT-A) and Fundus Fluorescein Angiography(FFA) in eyes with diabetic macular edema bythree independent observers in the form of greatest linear dimension(GLD), greatest horizontal diameter(GHD), greatest vertical diameter(GVD) and area of  FAZ in OCT-A and FFA.

Results:

The difference of averages of the parameters calculated by paired t-test analysis in OCT-A and  FFA was found to be statistically insignificant for GLD (p=0.253), FAZ Area (p=0.265), MHD(p=0.269) and MVD(p=0.585), with insignificant interobserver variation.  A statistically significant (p=0.023) positive correlation of  average FAZ area was seen with HbA1C andaverage GLD shows statistically significant variation with DM duration (p=0.045).

Conclusion:

OCT-A is a non-invasive technique to quantify FAZ for management of patients with DME.

Keywords:

Diabetic macular edema, foveal avascular zone, optical coherence tomography- angiography, fundus fluorescein angiography

INTRODUCTION

Diabetic retinopathy (DR) is a microangiopathy resulting from the chronic effects of the disease. Duration of the Diabetes Mellitus(DM) is the most important risk factor for DR.[1] The prevalence of diabetic retinopathy was found to be higher in women in the WESDR younger-onset group. However, in persons who have had diabetes for 19–20 years, 50% of men and 33% of women had proliferative retinopathy.[2],[3]

Vision loss in Diabetic retinopathy is most often caused by diabetic macular edema(DME).   There is increased incidence of Diabetic macular edema (DME) seen in type 2 diabetes mellitus (DM) than in type 1 DM.[4] Visual acuity of such patients is often dependent on the central foveal involvement, perifoveal capillary blood flow velocity, severity of perifoveal capillary occlusion, and retinal thickness at the central fovea.[5][6]

Diabetic macular ischemia (DMI) is an important feature of diabetic retinopathy (DR). DMI is defined by an enlargement of the foveal avascular zone (FAZ) including the widening of paramacular areas of capillary nonperfusion.[7]  It has been observed that approximately 41% of patients with DR in a tertiary hospital setting have some evidence of diabetic macular ischemia.[7] Recently, the RIDE and RISE trials analysis has shown that patients with DMI at baseline have progressed aggressively into proliferative changes seen in DR than those with normal perfusion at baseline seen during treatment with intravitreal ranibizumab.[8]  Hence it has become very important to have a baseline assessment of DMI status using Fundus Fluorescein Angiography(FFA) before initiating the intravitreal injection of ranibizumab. This clinically helps the physician for planning the review schedule for patients receiving intravitreal injections. The areas of the FAZ have been validated as “correlated markers.”[9-16] in determining the progression of Diabetic retinopathy.

Fundus Fluorescein angiography (FFA) is considered the gold standard in detecting and evaluating retinal perfusion in clinical practice. Leakage of dye in the late phases of FA, is usually associated with the presence of cystoid macular spaces, which is used to identify macular edema.[17] Assessment of the level of macular ischemia is very important in noting the clinical and prognostic information which helps in determining the disease severity and progression[7,18-19]

Optical Coherence Tomography (OCT) has emerged as an important imaging modality in the evaluation and management of retinal diseases. The application of OCT to management of DME has been very useful. The degree of DME and response to therapy can be quantified on OCT. Specifically, the central subfield thickness (CST) can be used to follow a patient’s response to treatment of DME.

The recent development of OCT angiography (OCT-A) allows for the visualization of the retinal capillary layers and for the construction of microvascular flow maps.[20-26]

In our study we have compared the Foveal Avascular Zone Characteristics  on Optical Coherence Tomography-Angiography and Fundus Fluorescein Angiography in Diabetic Macular Edema patients and we have correlated FAZ characteristics with vision and Foveal thickness.

MATERIALS AND METHODS

STUDY AREA–

The study was conducted in Aravind eye hospital, Coimbatore, Tamil Nadu, a tertiary eye care centre in Southern India catering services in specialities of ophthalmology.

STUDY POPULATION–

The study included urban, semi urban and rural population from in and around Coimbatore district. Data was collected from out-patients with diabetes mellitus attending retina clinic. Patients of both sexes were included in the study subject to inclusion and exclusion criteria.

STUDY PERIOD:-

The study was conducted between May 2016 to May 2017

STUDY DESIGN –

The study included a cross sectional comparative study design in patients with diabetic macular edema. In this study patients with diabetes mellitus with DME presenting to retina clinic out-patient department of Aravind Eye Hospital, Coimbatore were included, subject to the patient or their attendants signing the informed consent form.

Inclusion Criteria–

Established DM patients (type-2) with Diabetic Retinopathy seen on fundus examination and evidence of macular ischemia confirmed on FFA.

Age >18 years- must be able to provide informed consent.

Ready to undergo investigation by Fundus Fluorescence Angiography and Optical Coherence Tomography Angiography (OCT-A).

Exclusion Criteria–

  1. 6 months post-cataract surgery.
  2. Patients undergone previous retinal surgery or have had intravitreal injections.
  3. Patients with pathologic myopia.
  4. Patients with diabetes mellitus along with history of Ocular trauma.
  5. Patients with evidence of any other retinal vascular occlusions seen on fundus examination.
  6. Patients with glaucoma, optic nerve disorders causing visual loss.
  7. Patients with poor quality images on OCT angiography (signal strength index[SSI] lower than 50) owing to eye movements(un co-operative patients) or media opacities.
  8. Patients not willing to give written informed consent. 

STATISTICAL METHODOLOGY

SAMPLE SIZE CALCULATION–

It is observed from the hospital record that there are about 1600 patients coming to our opd with our specification in a year. This study is a cross sectional comparative study. Thus, the following formula was applied to predict the sample size.

Where:

Z = Z value
p = percentage picking a choice
c = confidence interval
ss = sample size

Correction for Finite Population

Where:

FSS = Final Sample Size, pop = Population
In order to estimate the sample size, the subsequent values are applied Z = 95%, p = 50%, c = 16%, pop = 1600 and it produce the final sample size as 38. Hence, 38 eyes with diabetic macular edema seen clinically and on OCT underwent FFA and OCT-A, and FAZ characteristics where compared of the two investigating modalities.

STUDY DETAILS–

At the presentation of the patient, a detailed medical and ocular history was taken, including the duration of visual loss and the presence of any ocular pathologies or prior interventions. All patients underwent following ophthalmic examination-

  1. Uncorrected and Best-corrected visual acuity measured on Snellen’s chart.
  2. Intraocular pressure(IOP) measurement by Goldmannapplanation tonometry.
  3. Anterior segment evaluation by Slit lamp Examination.
  4. Posterior segment evaluation with slit lamp biomicroscopy using 90 D lens and indirect ophthalmoscope using 20D lens with scleral indentation with special care taken to identify all DR changes.
  5. On confirming the diagnosis of diabetic macular edema and those patients who fulfilled the inclusion criteria were being informed about the study. A written consent was taken from these patients to be included in the study following which they subsequently underwent the following investigations:
  6. SD-OCT examination- Each macular thickness map was been divided into nine standard macular subfields, out of which only central 1.2 mm diameter of fovea was taken into consideration. The central subfield is defined as a central circular area that had a diameter of 1.2mm.
  7. FFA examination- patients with normal renal function test were injected with 3 ml of 20% sodium fluorescein solution intravenously. Hiedelberg (confocal scanning laser ophthalmoscope) was used for taking contrast adjusted images at approximately 1 second intervals, beginning 5-10 seconds after injection and continuing through the various phases. The images inArterio-venous phase were taken into consideration.
  8. OCT-A-The device (DRI OCT TRITON Plus) was used for getting OCT-A images. This device performs each acquisition at a speed of 100 000 A-scans per second, using a 1050 nm super luminescent diode and with a bandwidth of 45 nm; 320 A-scans made up a B-scan while 320 horizontal and vertical lines separated by 9 µm each were sampled in the scanning area in order to form a 3-dimensional data cube of 6×6 mm area. Volumetric raster scans were obtained from 2 horizontal fast transverse scans and 2 vertical fast transverse scans acquired in 3.4 seconds each. The calculated amplitude decorrelation signal from the consecutive B-scans allowed visualization of blood flow, and therefore the capillary network, to be clearly visualized.
  9. The FAZ Characteristics from superficial capillary plexus obtained by OCT-A was taken into consideration by three independent observers while comparing these OCT-A images of eyes with Diabetic macular edema with FFA image of the same eye. The deeper capillary plexus were not compared as in FFA only superficial capillary plexus are visible. Following are the FAZ characteristics-Greatest linear dimension(GLD)- Shown in Figure 1 and 2.
  1. Area- Shown in Figure 3 and 4.
  2. Maximum Horizontal diameter(MHD)- Shown in Figure 5 and 6.
  3. Maximum Vertical diameter(MVD)- Shown in Figure 7 and 8.

The means of these observed values derived from OCT-A and FFA is compared in our study.

Data Analysis-

Paired t-test was used to test mean difference between the two continuous variables. Analysis of variance (ANOVA) is used to assess the significant difference among two are more categories of independent variable over dependent variable. p value less than 0.05 was considered as statistically significant. All statistical analysis was done on statistical software SPSS 16.0.

Results-

In our study, we enrolled 38 eyes of 21patients with diabetic macular edema, out of which 7 patients were less than 51 yrs of age, 6 were between 51-60 yrs while remaining 8 patients were more than 60 yrs old. The mean age of 38 patients included in our study was 56.13 yrs, while the mean of DM Duration found in our study was 8.91.In our study only one eye with mild NPDR presented with diabetic macular edema while majority of eyes (21) had moderate NPDR. 9 eyes had severe NPDR while 7 eyes had PDR.The mean value observed for HbA1C in our patients was 9.32 with a standard deviation of 2.30 while those for BCVA and Macular thickness was 0.19 and 316.67 respectively with standard deviation of 0.20 for BCVA and 111.04 for macular thickness.The Average of Greatest linear dimension (AvGLD)  calculated from mean observations of three independent observers in OCT-A was 1074.17 micrometre while in FFA it was 1115.26 micrometre. Similarly the Average of FAZ areas in OCT-A was 0.642mm2and that in FFA was 0.686mm2.The average value of Maximum Horizontal Diameter of FAZ OCT-A was 949.55 micrometre while in FFA was 977.85 micrometre and the Average value of MVD of FAZ in OCT-A was 877.41 micrometre while in FFA was 886.23 micrometre.

In our study the comparison of average values done by paired t-test of all 38 eyes with respect to GLD seen in OCT-A and FFA showed insignificant difference with p-value of 0.253, similarly comparisons of average values of Area, MHD and MVD showed no significant difference with p-values of 0.265, 0.269 and 0.585 respectively. Also the interobserver variation was negligible.

In our study a positive correlation was noted between FAZ area of FFA, with HbA1C, while no correlation could be established between FAZ area seen in FFA with BCVA, macular thickness and DM duration.A similar positive correlation was noted between FAZ area of OCT-A with HbA1C as shown in table 1 and 2.

Discussion–

In our study we aimed at comparing the Foveal avascular zone characteristics in Optical coherence tomography- Angiography and Fundus fluorescein angiography in patients with Diabetic Macular Edema and correlating FAZ area with vision, diabetes mellitus duration, HbA1C and central macular thickness.

OCT-A is emerging as a new non-invasive imaging modality as compared to traditional FFA and is being used in studying the changes of Foveal Avascular Zone in various retinal vascular pathologies like Branch Retinal Vein Occlusion,[27]Central Retinal Vein Occlusion (CRVO),[28]Diabetic Macular Edema(DME)[29,30]  and is used subsequently for prognosticating, monitoring and planning treatment strategies for patients with these disorders.

The mean value observed for HbA1C in our patients was 9.32 with a standard deviation of 2.30 was found to have positive correlation with FAZ area, which is similar to the study conducted by Hemalatha B C etal.[31]However other studies showed no correlation of FAZ area with glycemic index of patients with DM.[32]

The mean values of BCVA and Macular thickness was 0.19 and 316.67 respectively and showed no correlation (p-0.994) of FAZ area with CMT in our study. A Study conducted by Wasim A. Samara et al[33]using OCT-Ain normal individuals showed a statistically significant (p<0.0001) negative correlation between the FAZ area and central macular thickness stating that greater the FAZ area, thinner will be the CMT.

The normal FAZ area observed using OCT-A as perAbtinShahlaeeet al[34]is  0.27 ± 0.101 mm2 and the normal MHD and MVD is  0.59 ± 0.126, and 0.56 ± 0.118, respectively as seen in healthy individuals. This value of FAZ area was found to be similar in another study conducted by Deepa Johnet al[35]in which they used contrast adjusted FFA on HRA-2  for measuring the FAZ area (0.2753 ± 0.074 mm2) in normal individuals, which shows that the two modalities of investigation are comparable indeed in normal individuals.

Inter-observer agreement calculated by intraclass correlation coefficient(ICC) for FAZ parameters was high (ICC ≥0.90) in the above mentioned study by Abtin Shahlaee et al.[34] This result is similar to our study where p-values (p>0.05) for all the intergroup comparative analysis were found to be statistically insignificant thereby increasing the reproducibility of observations included in our study.

In the 38 eyes enrolled in our study, the Average of Greatest linear dimension (AvGLD) calculated from mean observations of three independent observers in eyes with moderate NPDR on OCT-A was 1045.90±176.79 micrometre while in FFA it was 1058.17±196.74 micrometre. The values of AvGLD on FFA correlate well with the study conducted byHemalatha B C, Sathyendranath Shetty,[31] in which eyes with moderate NPDR had greatest linear dimension as1120±260 micrometer. Even though we included eyes of patients with different stages of Diabetic retinopathy like NPDR(mild, moderate, severe) and PDR, majority of the eyes(21) included in our study belonged to Moderate NPDR group.

The mean FAZ areas(in mm2) observed in FFA in different stages of DR in various other studies and our study is enlisted in the table [3], while that in OCT-A in mild, moderate and severe NPDR and PDR observed in our study are 0.31, 0.60, 0.83 and 0.54 mm2 respectively.

Takase Net al[30] compared FAZ area of normal eyes with that of diabetic eyes using OCT-A and found that there is significant increase in the size of FAZ of superficial area in Diabetic eyes with retinopathy and without retinopathy (0.37 ± 0.07 mm² and 0.38 ± 0.11 mm² respectively) as compared to FAZ area of normal eyes (0.25 ± 0.06 mm²). Our study showed increase in the mean area of FAZ seen in DME on OCT-A in the superficial capillary plexus and FFA was 0.642mm2 and 0.686mm2. These findings were higher than the normal values of FAZ area observed in the above mentioned studies.[34,35]

CONCLUSION–

OCT-A can be used as an equally reliable diagnostic tool as FFA in studying FAZ parameters in Diabetic macular edema.

FAZ area showed positive co-relation with glycemic index (HbA1C) but no statistically significant relationship with visual acuity, DM Duration and central macular thickness.

Inter-observer variations in calculation of values of FAZ parameters are insignificant thereby showing the values of the various parameters calculated in the study are reproducible.

The absolute values of FAZ area, maximum horizontal diameter and maximum vertical diameter are larger in Diabetic Macular Edema patients as compared with patients with diabetes with no retinopathy and normal healthy individuals.

References-

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Tables-

Table1: Showing correlation analysis between FAZ Area on FFA with BCVA, Macular thickness, HBA1C and DM Duration

Correlations Coefficient p-value
Av-FArea vs. BCVA -0.163 0.328
Av-FArea vs. Macular Thickness 0.001 0.994
Av-FArea vs. HbA1C (%) 0.407 0.023
Av-FArea vs. DM Duration 0.090 0.593

p-value £ 0.05 is significant

Table2: Showing correlation analysis between FAZ Area on OCT-A with BCVA, Macular thickness, HBA1C and DM Duration

Correlations Coefficient p-value
Av-OArea vs. BCVA -0.110 0.511
Av-OArea vs. Macular Thickness -0.128 0.455
Av-OArea vs. HbA1C (%) 0.403 0.024
Av-OArea vs. DM Duration 0.015 0.930

Table 3-Showing the FAZ area in FFA in Various studies in various stages of DR compared to our study.

Various studies by Mild NPDR Moderate-severe NPDR PDR
Conrath J et al[9] 0.30 0.42 0.61
Arend O et al[36] 0.318 0.513 0.590
Mansour et al[11] 0.737 1.001 0.866
Hemlatha et al[31]

 

 0.36mm2±0.12

 

 0.74mm2

±0.30

 1.33mm2

±0.39

 

 NA
Our Study 0.313mm2 0.62mm2

±0.20

 0.97mm2±0.62 0.56mm2±0.09

Figures-

                 Figure 1: Showing Greatest linear dimension of FAZ in OCT-A

      Figure 2: Showing Greatest linear dimension of FAZ in FFA

                       Figure 3: Showing FAZ Area on OCT-A

Figure 4: Showing FAZ Area in FFA

       Figure 5: Showing Maximum Horizontal Diameter of FAZ on OCT-A

 Figure 6: Showing Maximum Horizontal Diameter of FAZ in FFA

             Figure 7: Showing Maximum Vertical Diameter of FAZ in OCT-A

Figure 8: Showing Maximum Vertical Diameter of FAZ in FFA.

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