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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 3  |  Issue : 3  |  Page : 744-751

The role of optical coherence tomography angiography in early detection of primary open-angle glaucoma


Department of Ophthalmology, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt

Date of Submission01-Nov-2019
Date of Decision01-Nov-2019
Date of Acceptance18-Nov-2019
Date of Web Publication10-Feb-2020

Correspondence Address:
MB, BCh Israa M Bazeed
Department of Ophthalmology, Faculty of Medicine for Girls, Al-Azhar University, Cairo, 11754
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjamf.sjamf_94_19

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  Abstract 


Introduction Glaucoma is a slowly progressive disease with characteristic optic nerve abnormalities caused by accelerated ganglion cell complex (GCC) loss and concomitant retinal nerve fiber layer (RNFL) thinning. Glaucoma suspects are the key group to identify and treat with intraocular pressure lowering therapy in an effort to prevent blindness.
Aim Determination and correlation of the role of the whole image, peripapillary, and inside disk vascular density (%) (wiVD%, ppVD%, and idVD%) in the RNFL of optic nerve head by optical coherence tomography angiography (OCT-A) and their correlation to GCC and RNFL thickness by OCT in early detection of preperimetric primary open-angle glaucoma.
Patients and methods This prospective, nonrandomized, noninvasive, and observational case–control study was performed at the Ophthalmology Department and clinics of Al-Zahraa University Hospital, Al-Azhar University. It included 46 eyes of 23 participants who were divided into two groups: group I (control) consisted of 20 eyes of 10 healthy eyes. Group II (glaucoma suspects) consisted of 26 eyes of 13 preperimetric glaucoma suspects of the same age group. The peripapillary and inside disk optic nerve head vessel density were measured. Clinical data, visual field (VF) parameters, and spectral-domain OCT evaluation (RNFL thickness, GCC thickness, and rim area) were recorded.
Results Significant decreases were found in whole image, peripapillary, and inside disk vascular density (%) and RNFL thickness especially in the temporal side, GCC, VF mean deviation, and VF index in suspected eyes than the normal eyes indicating the presence of early vascular changes in glaucoma.
Conclusion OCT-A is a novel, noninvasive imaging technology that detects vascular changes as early signs in glaucoma disease progression; reduced vessel density also was associated with thinning of RNFL, and decrease in GCC count in a majority of cases. So, the diagnostic ability of OCT-A is a promising tool for early diagnosis of glaucoma.

Keywords: ganglion cell complex, glaucoma, intraocular pressure, optical coherence tomography angiography, retinal nerve fiber layer


How to cite this article:
Bazeed IM, Mahmoud DA, Hasan ZS. The role of optical coherence tomography angiography in early detection of primary open-angle glaucoma. Sci J Al-Azhar Med Fac Girls 2019;3:744-51

How to cite this URL:
Bazeed IM, Mahmoud DA, Hasan ZS. The role of optical coherence tomography angiography in early detection of primary open-angle glaucoma. Sci J Al-Azhar Med Fac Girls [serial online] 2019 [cited 2020 Feb 29];3:744-51. Available from: http://www.sjamf.eg.net/text.asp?2019/3/3/744/278057




  Introduction Top


Glaucoma is a progressive optic neuropathy characterized by a particular pattern of optic disk changes and damage and visual field (VF) loss [1]. Glaucoma suspects are the key group to identify and, in some cases, treat with intraocular pressure (IOP)-lowering therapy in an effort to prevent blindness [2].

There is evidence suggesting that glaucoma pathogenesis is related to vascular dysfunction. Also, there is a lack of adequate techniques for the study of ocular blood flow despite different measurement tools. This makes it reasonable to search for new methods of vascular bed visualization for the early diagnosis and monitoring of glaucoma [3]. Optical coherence tomography (OCT) is used for the diagnosis and management of glaucoma. A new method, optical coherence tomography angiography (OCT-A), has been recently introduced which allows measuring vessel density in the retina and the choroid in the peripapillary and macular areas using high-speed OCT to perform quantitative angiography [4].


  Aim Top


Determination and correlation of whole image, peripapillary, and inside disk vascular density (%) (wiVD%, ppVD%, and idVD%) in the retinal nerve fiber layer (RNFL) of optic nerve head (ONH) by OCT-A to ganglion cell complex (GCC) and RNFL thickness by OCT in early detection of preperimetric primary open-angle glaucoma (POAG).


  Patients and methods Top


This prospective, nonrandomized, noninvasive, and observational case–control study was performed at the Ophthalmology Department and clinics of Al-Zahraa University Hospital, Al-Azhar University, Cairo from December 2018 to September 2019.

The study included 46 eyes of 23 participants who were divided into two groups:
  1. Group I (control): consisted of 20 eyes of 10 healthy participants more than 40 years old, without ocular diseases with normal IOP and VF.
  2. Group II (glaucoma suspects): consisted of 26 eyes of 13 preperimetric glaucoma suspects aged more than 40 years. Glaucoma suspect is any person who has glaucomatous optic neuropathy or suspicious appearing optic disk based on stereoscopic photography and/or ocular hypertension with an IOP more than 21 mmHg without evidence of glaucomatous VF damage (repeated).


Exclusion criteria

  1. Intraocular surgery (except uncomplicated cataract).
  2. Coexisting retinal pathology.
  3. Nonglaucomatous optic neuropathies.
  4. Uveitis.
  5. Unreliable VF.
  6. Myopia more than −6.


The study was approved by the Ethics Board of Al-Azhar University and was conducted in accordance with the World Medical Association Declaration of Helsinki Guidelines. All participants received a full explanation about the study and signed written informed consent.

For both groups the following data were recorded:
  1. Age, sex, best-corrected visual acuity on a logarithmic scale, IOP (mmHg), central corneal thickness, gonioscopy, and cup/disk ratio. IOP was measured using the Goldmann applanation tonometer.
  2. Computerized VF perimetry tests using Zies Humphery Visual Field Analyzer − II model 745 I (Humphrey Instrument Carl Zeiess Meditec Inc., Dubin, California, USA). Central 24-2 degree program with SITA-standard algorithm. Mean deviation, pattern standard deviation, glaucoma hemifield test, and significant scotomata.
  3. OCT and OCT-A using SD-OCT and OCT-A wide-field imaging system (RTVue XR Avant Optovue − Angiovue Inc., Fremont, California, USA) software version (2016-2).
    1. OCT parameters were average RNFL (μm), all ONH analysis parameters [cup/disk area ratio, cup/disk vertical ratio, cup/disk horizontal ratio, rim area (mm2), disk area (mm2), and cup volume (mm3)] and average GCC (μm).
    2. OCT-A of optic disk using HD Angio Disc 4.5 mm. Red blood cell density (%) in wiVD, ppVD, idVD, superior-hemi, and inferior-hemi are the parameters used (capillary and all).


Statistical analysis

Data were collected and entered into the Statistical Package for the Social Sciences (IBM SPSS), version 23 (IBM Corp. Released 2015, IBM SPSS Statistics for Windows, Version 23.0, Armonk, NY: IBM Corp.).

Comparison between groups regarding qualitative data was done using the χ2 test and/or Fisher’s exact test when the expected count in any cell was found to be less than 5 and regarding quantitative data and parametric distribution it was done using an Independent t test while with nonparametric distribution was done using the Mann–Whitney test.

The P value was considered significant as the following:
  1. More than 0.05: nonsignificant (NS).
  2. Less than 0.05: significant (S).
  3. Less than 0.01: highly significant (HS).



  Results Top


Demographic and clinical data

The study included 46 eyes of 23 participants, 34 eyes of 17 women and 12 eyes of six men. There is no significant difference among the two groups as s age (P=0.694) or sex (P=0.123), and ethnic origin.
  1. Best-corrected visual acuity shows NS difference between the two groups with a P value of 0.516.
  2. IOP shows S difference between the two groups, the P value is 0.014.
  3. C/D ratio shows HS toward group II, the P value is 0.000, ranging from 0.3to 0.6 in group II and from 0 to 0.3 in group I.


Visual field

  1. The mean deviation of group II is −0.49±1.31 dB ranging from −3.5 to 2.92 dB and of group I is 0.32±1.18 dB ranging from −0.98to 2.82 dB. This shows the S difference between the two groups with a P value of 0.038.
  2. Pattern standard deviation was NS in both groups, P value is 0.319, indicating no VF changes.
  3. Glaucoma hemifield test shows HS difference between the two groups. Four (15.4%) eyes show a general reduction of sensitivity, six (23.1%) eyes show a borderline reduction, and 16 (61.5%) eyes were within normal limits in group II. All group I are within normal limits.


Ganglion cell complex analysis in optical coherence tomography

  1. The mean of average GCC in group II is 92.12±5.83 μm ranging from 79 to 101 μm. The mean of group I is 99.50±10.64 μm ranging from 90 to 141 μm. This shows the HS difference, the P value is 0.004, indicating a decrease in GCC in the suspected eyes which is present in 14 (53.8%) eyes of the 26 suspected eyes.


[Table 1]
Table 1 Optical coherence tomography of ganglion cell complex in groups I and II

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Retinal nerve fiber layer analysis in optical coherence tomography

  1. The mean of average RNFL thickness in group II is 99.85±7.34 μm ranging from 78 to 114 μm. The mean of group I is 105.05±5.43 μm ranging from 92 to 114 μm. This shows the HS difference, the P value is 0.005, indicating early affection of RNFL in suspected eyes which is present in 15 (57.7%) eyes of the total of 26 suspected eyes mostly in the inferior quadrant of the optic nerve.


[Table 2]
Table 2 Optical coherence tomography of retinal nerve fiber layer analysis of groups I and II

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Optic nerve head blood flow evaluation

  1. The mean of wiVD (capillary) in group II is 48.48±2.72% ranging from 41.5 to 54.6%. The mean of group I is 51.17±2.46%, ranging from 46.1 to 55.8%. This shows the HS difference, the P value is 0.001. Twenty-five eyes among the suspected eyes show a decrease in this parameter than the mean of the normal eyes.
  2. The mean of wiVD (all) in group II is 55.27±2.80% ranging from 47.8 to 60.5% and the mean of group I is 57.32±2.14% ranging from 52.6 to 60.1%. This shows HS difference, the P value is 0.010. Twenty eyes among the suspected eyes show a decrease in this parameter than the mean of the normal eyes.
  3. The mean of idVD (capillary) in group II is 46.83±6.40% ranging from 35.3 to 60% and the mean of group I is 51.37±4.23% ranging from 41.2 to 58.3%, the P value is 0.009. Eleven eyes among the suspected eyes showed a decrease in this parameter than the mean of the normal eyes.
  4. The mean of idVD (all) in group II is 57.15±5.76% ranging from 42.9 to 68.3% and the mean of group I is 60.89±3.04% ranging from 55.2 to 65.4%, the P value is 0.012. Eighteen eyes among the suspected eyes show a decrease in this parameter than the mean of the normal eyes.
  5. The mean of ppVD (capillary) in group II is 51.21±3.05% ranging from 43.5 to 56.1% and the mean of group I is 53.78±3.65% ranging from 47.2 to 60.4%, the P value is 0.013. Twenty-one eyes among the suspected eyes show a decrease in this parameter than the mean of the normal eyes.
  6. The mean of ppVD (all) in group II is 57.72±3.42% ranging from 49.7 to 65.6% and the mean of group I is 59.97±2.62% ranging from 55.6 to 65.9%, the P value is 0.019. Eighteen eyes among the suspected eyes showed a decrease in this parameter than the mean of the normal eyes.


[Table 3]
Table 3 Optical coherence tomography angiography of optic nerve head in groups I and II

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Optical coherence tomography angiography of the superior and inferior halves of optic disk

  1. In the superior-half of optic nerve (capillary), the mean of group II is 51.51±3.25% ranging from 44.7 to 56.4% while the mean of group I is 54.58±3.97% ranging from 47.6 to 64.5%, the P value is 0.006.
  2. In the superior-half of optic nerve (all), the mean of group II is 58.16±3.09% ranging from 50.7 to 63% while the mean of group I is 60.81±3.45% ranging from 55.4 to 69.7%, the P value is 0.009.
  3. In the inferior-half of optic nerve (capillary), the mean of group II is 50.40±3.52% ranging from 42 to 57.3% while the mean of group I is 53.45±3.07% ranging from 47.4 to 60.9%, the P value is 0.004.
  4. In the inferior-half of optic nerve (all), the mean of group II is 56.82±3.59% ranging from 48.6 to 65.4% while the mean of group I is 59.42±2.43% ranging from 54.8 to 63.7%, the P value is 0.008.


[Table 4]
Table 4 Optical coherence tomography angiography of superior-hemi and inferior-hemi of the optic nerve in groups I and II

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Filling defects in optical coherence tomography angiography

OCT-A of the suspected eyes showed 16 (38.5%) eyes of 26 with filling defects indicating early vascular changes in these suspected eyes. There are no filling defects in group I ([Table 5], [Figure 1],[Figure 2],[Figure 3]).
Table 5 Percent of eyes with filling defects by optical coherence tomography angiography between the suspected eyes

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Figure 1 OU OCT of ONH GCC and RNFL of a glaucoma suspect. GCC, ganglion cell complex; OCT, optical coherence tomography; ONH, optic nerve head; RNFL, retinal nerve fiber layer.

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Figure 2 OD OCT-A on ONH of a glaucoma suspect. OCT-A, optical coherence tomography angiography; ONH, optic nerve head.

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Figure 3 OS OCT-A on ONH of a glaucoma suspect. OCT-A, optical coherence tomography angiography; ONH, optic nerve head.

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  Discussion Top


Early diagnosis and treatment of glaucoma were found to reduce the rate of disease progression and improve patients’ quality of life. OCT and OCT-A are playing an increasing role in glaucoma diagnosis, monitoring of disease progression, and quantification of structural damage [5].

In our study, OCT of average RNFL analysis shows HS decrease in group II (the mean is 99.85±7.34 µm) than in group I (the mean is 105.05±5.43 µm). Eyes outside the normal RNFL limits were 57.7% of the suspected eyes.

Aydogan et al. [6], Xu et al. [7], Rolle et al. [8], Kim et al. [9], and Stefanova et al. [10] agree with our study results in average RNFL analysis. Lisboa et al. [11] added that the early decrease in RNFL curve is in the inferior quadrant.

In our study, average GCC analysis is lower in group II (the mean is 92.12±5.83 µm) than in group I (the mean is 99.50±10.64 µm), indicating a decrease in GGC in suspected eyes. Eyes outside the normal GCC limits were 53.8% of the suspected eyes.

This agrees with Aydogan et al.[6], Lisboa et al. [11], Xu et al. [7], Rolle et al. [8], and Stefanova et al. [10] who stated that the mean of average GGC analysis is lower in suspected eyes than in normal eyes.

Our results showed HS P value in wiVD% (capillary) (mean of group II is 48.48±2.72% and of group I is 51.17±2.46%) and S P value in wiVD% (all) (mean of group II is 55.27±2.80% and of group I is 57.32±2.14%).

idVD % (capillary) showed HS P value (the mean of group II is 46.83±6.40% and of group I is 51.37±4.23%) and S P value in idVD% (all) (the mean of group II is 57.15±5.76% and of group I is 60.89±3.04%).

ppVD % (capillary) showed S P value (mean of group II is 51.21±3.05% and of group I is 53.78±3.65%). ppVD% (all) showed S P value (mean of group II is 57.72±3.42% and of group I is 59.97±2.62%).

This agrees with Rolle et al. [8] who stated that global and regional vessel densities showed reduced values in suspected eyes compared with normal eyes, even if of small entities for some parameters. But the Rolle et al. [8] study results disagree with our study result in ppVD% in suspected eyes, where the mean is nearly equal in both groups with nonsignificant P value.In accordance with our results, Kim et al. [9] stated that ppVD% in suspected eyes is lower than normal eyes and the vessel density at the area of RNFL defect in suspected eyes was significantly different from that in normal eyes.

In our study, defects and cutoffs in optic nerve vascular map represent 61.5% of all suspected eyes (including wiVD, idVD, and ppVD).

This is correlated by Rolle et al. [8] who found a moderate correlation between RNFL and perfusion of the retina. Although this association is still debated, this might be very helpful in early POAG glaucoma diagnosis.

Kim et al. [9] stated that ppVD% in suspected eyes is lower than normal eyes and the vessel density at the area of RNFL defect in suspected eyes was significantly different from that in normal eyes.

Yarmohammadi et al. [12] demonstrated that the vessel density measured in the RNFL was statistically different among the two groups. Also decreased vessel density was significantly associated with the severity of VF damage independent of the structural loss.

Hou et al. [13] and Shoji et al. [14] noted that about one-third of the suspected eyes showed a greater percent loss of VD than GCC thickness. So it is clear that there are some eyes in which microvascular attenuation occurs before changes in RNFL thickness or function. Thus, OCT-A can help detect early stages of glaucoma in some eyes.

In our study, superior and inferior halves of optic disk vascular density show HS difference between suspected eyes and normal eyes.

Rolle et al. [8] stated that ppVD appeared significantly reduced in the inferior-nasal, inferior-temporal, and nasal sectors. Kim et al. [9] stated that inferotemporal and superonasal VD in suspected eyes is lower than healthy eyes with significant P value, which agrees with our study results.

Yarmohammadi et al. [12] found that there is significantly better diagnostic accuracy of wiVD compared with ppVD for differentiating between healthy and suspected groups.


  Conclusion Top


OCT-A is a novel noninvasive imaging technology that provides insight into the role of microvascular changes during the glaucoma process. It can detect POAG and roles out the conflict of glaucoma suspect. It shows a potential to become a part of everyday glaucoma detection, management, and follow-up.

We found vascular cutoffs and a decrease in wiVD%, ppVD%, and idVD% analyzed with OCT-A in suspected eyes suggesting that vascular changes may develop early in POAG disease. This is associated with thinning of RNFL, especially in the temporal side, and a decrease in GCC in majority of cases.

Recommendations

OCT-A ONH must be routinely performed to any glaucoma suspect for early detection of vascular changes in the optic nerve to diagnose POAG before the occurrence of VF changes. Also, it may be used in monitoring the progression of mild and moderate disease stages and to analyze the potential effect of medical and topical therapy. All OCT-A parameters should be correlated with clinical and perimetric data.

Financial support and sponsorship

Nil.

Conflicts of interest

None declared.



 
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Aydogan T, Akçay BIS, Kardeş E, Ergin A. Evaluation of spectral-domain optical coherence tomography parameters in ocular hypertension, preperimetric, and early glaucoma. IJO 2017; 65:1143–1150.  Back to cited text no. 6
    
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Xu XY, Xiao H, Luo JY, Liu X. Evaluation of spectral-domain optical coherence tomography parameters in discriminating preperimetric glaucoma from high myopia. Int J Ophthalmol 2019; 12:58–65.  Back to cited text no. 7
    
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Kim SB, Lee EJ, Han JC, Kee C. Comparison of peripapillary vessel density between preperimetric and perimetric glaucoma evaluated by OCT-angiography. PLoS One 2017; 12:e0184297.  Back to cited text no. 9
    
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Lisboa R, Paranhos A Jr, Weinreb RN, Zangwill LM, Leite MT, Medeiros FA. Comparison of different spectral domain OCT scanning protocols for diagnosing preperimetric glaucoma. IOVS 2013; 54:3417–3425.  Back to cited text no. 11
    
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Yarmohammadi A, Zangwill LM, Diniz-Filho A, Suh MH, Manalastas PI, Fatehee N et al. Optical coherence tomography angiography vessel density in healthy, glaucoma suspect, and glaucoma eyes. Invest Ophthalmol Vis Sci 2016; 57:OCT451–OCT459.  Back to cited text no. 12
    
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Hou H, Moghimi S, Zangwill LM, Shoji T, Ghahari E, Manalastas PIC et al. Inter-eye asymmetry of optical coherence tomography angiography vessel density in bilateral glaucoma, glaucoma suspect, and healthy eyes. Am J Ophthalmol 2018; 190:69–77.  Back to cited text no. 13
    
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Shoji T, Zangwill LM, Akagi T, Saunders LJ, Yarmohammadi A, Manalastas PIC et al. Progressive macular vessel density loss in primary open-angle glaucoma: a longitudinal study. Am J Ophthalmol 2017; 182:107–117.  Back to cited text no. 14
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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