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Dr. SWATI PHULJHELE

Dr.SUMANT SHARMA, Dr. ROHIT SAXENA, DR. AMAR PUJARI

Semi Final

Abstract

Purpose: To study the long term microvasculature changes at macula and the optic disc in eyes with non-arteritic anterior ischemic optic neuropathy (NAAION).

Methods: Patients with acute NAAION of less than 6 weeks duration were included. Optical coherence tomography angiography (OCTA) of the macula and the optic disc were performed at baseline, 3 and 6 months and compared with the controls.

Results: The mean age of 15 patients was 52.25 (± 9.06) years. The whole image superficial peripapillary and radial capillary densities were less than controls at presentation and then progressively decreased at 3 &amp; 6 months (P<0.05). There was decrease in superficial capillary plexus (SCP) at macula at presentation as compared to controls. Conclusions: In a 6 months observation of acute NAAION eyes, the peripapillary capillary densities show progressive loss.

Full Text  

Evaluation of Optical Coherence Tomography – Angiography (OCT-A) changes in Non-Arteritic Anterior Ischemic Optic Neuropathy (NAION)

Type: Original Article

Authors:

  1. Swati Phuljhele, MD
    Addl Professor,
    Neuro-ophthalmology and Strabismus Services
    Dr Rajendra Prasad Centre for Ophthalmic Sciences,
    All India Institute of Medical Sciences, New Delhi.
  2. Sumant Sharma, MD
    Neuro-ophthalmology and Strabismus Services
    Dr Rajendra Prasad Centre for Ophthalmic Sciences,
    All India Institute of Medical Sciences, New Delhi.
  3. Rohan Chawla
    Addl Professor,
    Retina Services
    Dr Rajendra Prasad Centre for Ophthalmic Sciences,
    All India Institute of Medical Sciences, New Delhi.
  4. Amar Pujari
    Assist. Professor,
    Neuro-ophthalmology and Strabismus Services
    Dr Rajendra Prasad Centre for Ophthalmic Sciences,
    All India Institute of Medical Sciences, New Delhi.
  5. Rohit Saxena, PhD.
    Professor
    Neuro-ophthalmology and Strabismus Services
    Dr Rajendra Prasad Centre for Ophthalmic Sciences,
    All India Institute of Medical Sciences, New Delhi.

Corresponding Author:
Swati Phuljhele
Dr Rajendra Prasad Centre for Ophthalmic Sciences,
All India Institute of Medical Sciences, New Delhi
Ph no: 01126591383, Fax:26588919
Email: drmsswati@rediffmail.com

No of pages: 10
Word Count for text (excluding abstract, references, and tables): 3331
Word count for abstract: 120
No of tables: 5

Financial Disclosure: None of the authors have any financial interest regarding the current manuscript

Purpose:
To study the long term microvasculature changes at macula and the optic disc in eyes with non-arteritic anterior ischemic optic neuropathy (NAION).

Methods:
Patients with acute NAION of less than 6 weeks duration were included. Optical coherence tomography angiography (OCTA) of the macula and the optic disc were performed at baseline, 3 and 6 months and compared with the controls.

Results:
The mean age of 15 patients was 52.25 (± 9.06) years. The whole image superficial peripapillary and radial capillary densities were progressively decreased at 3 & 6 months (P<0.05). There was decrease in superficial capillary plexus (SCP) at macula at presentation.

Conclusions: In a 6 months observation of acute NAION eyes, the peripapillary capillary densities show progressive loss.

Introduction

Non-Arteritic Anterior Ischemic Optic Neuropathy (NAION) is the commonest acute optic neuropathy above the age of 50 years1. The underlying pathology in case of NAION is vascular insufficiency in the optic nerve head (ONH), secondary to a fall in perfusion pressure in posterior ciliary Arteries2. Several modalities like; fluorescein angiography, indocyanine green angiography and doppler have been used to study the vascular pattern of disc in cases of NAION however none of them could detect the vascular pattern at different layers. Optical Coherence Tomography- Angiography (OCT-A) is a non-invasive modality, that allows visualisation of retinal vasculature at different levels. The pattern of microvascular loss, can help in understanding the anatomical basis of pathological process.

Studies have documented presence of vascular loss increase in non-perfusion area on OCTA in NAION patients when compared to control eyes in both acute and chronic phase. 3-7 OCTA has also been used to differentiate NAION from papillitis and papilloedema. 5, 8 Fard MA et al 8 found reduced peripapillary microvascular density in acute cases as compared to acute papillitis and papilloedema cases, and found no reduction in papilloedema, in contrast to papillitis that showed similar reduction in density as NAAION.

Few studies have evaluated the choroidal vasculature in NAION patients with variable results. U Gandhi et al 5 found 2 distinct patterns of microvasculature loss at choroidal level – diffuse loss of peripapillary cuff( in all the patients), and sectoral loss of vasculature (57.14% of patients) in acute cases. Wright Mayes E et al 3 in their retrospective, cross-sectional study of 10 eyes described qualitative alterations in peripapillary vasculature, at the level of radial peripapillary capillary (RPC) and choriocapillaris(PCC). Dhiman R. et al 9 in their series of 10 eyes in non-acute phase found significant difference in superficial microvascular density around the disc. However at the level of choroid, the difference was not significant.

Moreover the macular plexus have also been shown to have vascular changes in cases of NAION. Z Y Tao et al10 and Augstburger E et al 11 found reduced density in superficial plexus and both superficial and deep plexus layer respectively, at macula. On the other hand, Chun-Hsiu Liu et al12, 13 did not find a significant decrease in macular density in chronic stage.

This loss of vascular plexus at disc, peripapillary area and macula could be the cause or the consequence of the ischemic pathology of NAION. This study aims to evaluate the natural course of the pattern of the vascular loss around disc and at macula.

Materials & Methods

This was a prospective, observational longitudinal study conducted over a period of two years at a tertiary eye care centre. Institute ethical clearance was obtained, and the study followed the tenets of the declaration of Helsinki.

Patients presenting to the neuro-ophthalmology clinic of our centre were evaluated, and subsequent to the fulfilment of inclusion criteria were enrolled in the study. Informed consent was obtained from all the participants of the study.

The patients of diagnosed as unilateral NAION on the basis of clinical features; age 40-80 years, unilateral acute painless visual loss associated with swollen disc, presence of relative pupillary defect; presenting within 6 weeks of onset of symptoms. Patient underwent ESR, CRP to rule out arteritic AION. The exclusion criteria included all other optic neuropathies ruled on the basis of visual field (whenever possible) and neuro-imaging (whenever indicated). Presence of glaucoma or other causes of retinopathy (except grade I hypertensive retinopathy), intraocular surgery (except cataract surgery) and myopia of >6D was excluded. The fellow eyes of these patients were also included in the study.

Healthy, age matched controls were included if they had a normal fundus examination, refractive error between +5 to -5 Dioptres, normal intraocular pressure (< 21 mm hg), no visual field defect, normal RNFL and GCL thickness, open angle on gonioscopy, and no previous history of ocular surgery (except uncomplicated cataract surgery with a posterior chamber intraocular lens).

The 15 eyes of 15 age matched control were also recruited.

Patients and control underwent complete ocular examination, visual acuity assessment on logMAR chart and OCTA. The enrolled patients were followed up twice, at 3 months and 6 months from first presentation and OCTA was done on each follow up visit.

All patients and controls underwent SS-OCT-A on the Topcon Swept Source DRI OCT TritonTM (TOPCON MEDICAL SYSTEMS, INC). The scans are performed utilizing a 1050 nm wavelength light source, and a scan speed of 100,000 A- Scans per second. The higher wavelength provides deeper penetration and less light scattering. The 1,050nm light source is invisible to the human eye, and allows fixation of the patients on the provided target.

The scans were performed at macula and at optic disc (4.5 mm x 4.5 mm). All scans were performed by an experienced operator. The patients underwent pupillary dilation with 1% tropicamide drops prior to the exam. The scans that had an image quality >50 were included for the study. In case of motion artifacts and poor fixation the scans were repeated till a satisfactory scan was acquired.

Automated segmentation of layers was done, as provided by the device. The segmentation was manually adjusted in case of optic disc edema that interfered in automatic segmentation of vascular slab. The macular scans did not require manual adjustment.

The enface images for macular scan were at the level of superficial plexus, deep plexus and choriocapillaris; ONH scan enface images were segmented at ONH, radial peripapillary capillary layer and choriocapillaris layer. These were automatically defined by the IMAGEnet 6 software.

All retrieved images were processed using the ImageJ software(National Institutes of Health, Bethesda, Maryland). This was done to quantitatively measure the microvascular density at various levels. The images were first converted to 8- bit image to enable application of thresholding algorithm. In peripapillary scans, the first step was to remove the large vessels in the image to accurately isolate the microvascular network. This was achieved by applying “Minimum” auto global thresholding algorithm that resulted in an outline of only the major vessels, in a binarized image that showed them as white lines on a black background (figure 3).

Using the histogram option, the number of pixels that were white (represented as 255 in the histogram list) was noted. The enface image was now opened in another window and subjected to the Phansalkar’s local thresholding algorithm. Phansalkar is a local auto thresholding algorithm that is well suited for low contrast settings. It was originally described for use in cytological analysis and is a modification of Sauvola’s local thresholding method. Using the histogram analysis, the number of white pixels were again noted and the white pixels calculated from prior global thresholding, that represented large vessels, were subtracted from this.

Lastly, the ratio of this corrected value of white pixels to the total number of pixels was calculated, and this was recorded as whole image microvascular density (in %). This method of removal of large vessels was necessary at superficial macular plexus, at ONH superficial plexus and at radial peripapillary capillary layer.

The above method yielded microvascular densities(%) at various levels, which were recorded and compared over subsequent visits. In the peripapillary scans, microvascular density was recorded at superficial(ONH) level, at the level of radial peripapillary network and the level of choriocapillaris. Similarly, in macular scans, the microvascular density was recorded at superficial capillary plexus, deep macular capillary plexus and at the level of choriocapillaris. The final parameters used for statistical analysis were following:

  • – Whole image superficial peripapillary density (wiSPD)
  • – Whole image radial peripapillary capillary density (wiRPC)
  • – Whole image peripapillary choriocapillaris density (wiPCC)
  • – Whole image superficial macular density (wiSMD) at the level superficial plexus
  • – Whole image deep macular density (wiDMD) at the level deep plexus
  • – Whole image macular choriocapillaris density (wiMCC) – at the level of choriocapillaries

All observational data was compiled into an excel sheet, and statistical analysis was done using IBM Statistical Package for Social Science (SPSS) Statistics version 27. Inter-group analysis was performed using independent samples T- test for parameteric values and Two- sample Wilcoxon rank-sum (Mann-Whitney) test for non- parametric values; for intra-group analysis paired sample T- test and Wilcoxon sign-ranked test was conducted. A p value of < 0.05 was considered as significant.

Results

This study recruited 15 eyes of 15 patients with acute NAAION (defined as < 6 weeks from onset). 3 patients could not follow up at 6 months owing to COVID-19 pandemic and hence were excluded from 6 month analysis. The mean time of presentation from onset of symptoms was 3.89 weeks ± 1.69.

Table 1 gives the demographic details of the patients.

Characteristics Patients Control p =
Age 52.25 ± 9.06 52.66 ± 9.37 > 0.05
Male : Female 10:05 08:07 > 0.05
LogMAR BCVA 1.0928 ± 0.63 0 <0.001

Seven patients had hypertension. Out of these, one patient was also suffering from coronary artery disease, while two had controlled type II DM. Two patients were suffering only from type II DM and had adequate glycemic control on oral medications. Three patients were found to have raised homocysteine levels on evaluation; there were no other systemic abnormalities detected in them.

Swept Source OCT- A parameters

  1. Peripapillary microvasculature assessment
      2. a. Whole image superficial (ONH) peripapillary density (wiSPD): At presentation the mean wiSPD in the affected eyes was 42.49 ± 5.28. The density was significantly reduced when compared to controls 46.36 ± 2.09 (Table 2) p value = 0.015, which reduced further at 3 months and 6 months. (Table 3)
      b. Whole image radial peripapillary capillary density ( wiRPC): At presentation the mean wiRPC in the affected eyes was 49.35± 5.64. The density was significantly reduced when compared to controls, 53.45± 1.96 (Table 2) ( p value = 0.012) . Further significant reduction in the density was seen on subsequent follow up (Table 3)
      c. Whole image peripapillary choriocapillaris density : The mean wiPPC in the affected eyes at presentation was 55.23± 4.51. The density was significantly reduced when compared to controls 60.60 ± 3.17 (Table 2). However it showed significant improvement at 3 months and stabilized there after at 6 months. (Table 3)

    Table 2 shows the comparison of various peripapillary vasculature parameters between the NAION eyes at presentation and control eyes

    Parameters NAION (n=15) Control (n=15) P value
    wiSPD 42.49 ± 5.28 46.36 ± 2.09 0.015
    wiRPC 49.35± 5.64 53.45± 1.96 0.012
    wiPCC 55.23± 4.51 60.60 ± 3.17 < 0.001

    Table 3: Trend of change in peripapillary vasculature in NAION eyes. The p value provided is for change from respective previous value for each parameter.

    Parameters(in Mean ± SD) Baseline (n=15) At 3 months (n=15) At 6 months (n=12)
    wiSPD 42.49 ± 5.28 36.58 ± 3.29 (p=< 0.001) 35.66 ± 2.93 (p=< 0.001)
    wiRPC 49.35± 5.64 44.64 ± 4.2 (p=< 0.001) 43.99 ± 4.78 (p=< 0.02)
    wiPCC 55.23± 4.51 59.219 ± 3.19 (p=< 0.03) 60.48 ± 2.73 (p=< 0.2)
  2. Macular microvasculature assessment
      3. a. Whole image superficial macular density (wiSMD): At presentation the mean wiSMD in affected eyes was 41.83 ± 3.64. The density was significantly reduced when compared to controls 47.30 ± 2.04 (Table 4). It remained stable at 3 and 6 months although still significantly less than the control group. (Table 5)
      b. Whole image deep macular density (wiDMD) : At presentation the mean wiDMD in affected eyes was 52.15 ± 4.84. The density was significantly reduced when compared to controls 55.13 ± 1.81. (Table 4). There was no significant subsequent change on 3 & 6 month follow up visit and remained significantly less than controls. (Table 5)
      c. Whole image macular choriocapillaris density (wiMCC): At presentation the mean wiMCC in the affected eyes was 62.10 ± 5.95. The density was not significantly different from the control group 62.48 ± 2 (Table 4). No further change was seen in wiMCC on subsequent follow and it remained at par with the control group. (Table 5)

    Table 4 shows the comparison of various macular vasculature parameters between the NAION eyes at presentation and control eyes

    Parameters NAION (n=15) Control (n=15) P value
    wiSMD 41.83 ± 3.64 47.30 ± 2.04 0.001
    wiDMD 52.15 ± 4.84 55.13 ± 1.81 0.035
    wiMCC 55.23± 4.51 60.60 ± 3.17 < 0.001

    Table 5: Trend of change in macular vasculature in NAION eyes. The p value provided is for change from respective previous value for each parameter.

    Parameters(in Mean ± SD) Baseline (n=15) At 3 months (n=15) At 6 months (n=12)
    wiSMD 41.83 ± 3.64 42.03 ± 3.3 (p > 0.05) 42.88 ± 2.93 (p > 0.05)
    wiDMD 52.15 ± 4.84 51.67 ± 3.37 (p > 0.05) 52.43 ± 3.28 (p > 0.05)
    wiMCC 62.10 ± 5.95 62.42 ± 5.76 (p > 0.05) 60.48 ± 2.73 (p > 0.05)

Discussion

The pathogenesis for NAION was described by Hayreh utilising fluorescein angiography who suggested that the transient hypoperfusion of ONH leads to neuronal ischemia, and consequently neuronal death. The vascular basis of pathology, though firmly established, however was still not discerned at the microvascular level owing to a lack of modalities that could study them. With the advent of optical coherence tomography- angiography (OCT-A), a detailed analysis of retinal and choroidal microvasculature is possible. OCT-A also provides a quantitative assessment of microvasculature that make is more objective evaluation.

Multiple OCTA machines and their built-in proprietary software give quantitative measures of microvascular density [ eg. Cirrus (AngioPlex software, Carl Zeiss Meditec, Inc., Dublin, CA, USA), AngioVue software (Optovue, Inc., Fremont, CA, USA), RS -3000 Advance (Nidek, Gamagori, Japan), and OCTARA (Topcon Corporation, Tokyo)] have been noted to have good repeatability between tests14. In platforms where proprietary software is not available, or where further refinement in density measurement is essential, images are exported and processed by variety of thresholding algorithms, using another software (for example, ImageJ – NIH, Bethesda,MD).

Rabiolo et al15 compared various methods to quantify microvascular density in macular and peripapillary area using OCT-A. They concluded that absolute density values are not interchangeable between different methods, and hence normative database for one method cannot be compared with other. The longitudinal monitoring of vessel density however, can be achieved using the same algorithm if same instrument with same scan pattern and location is used.

The aim of this study was to evaluate longitudinal changes occurring in microvascular density in the peripapillary and macular vascular plexuses, over the course of 6 months using OCT-A. to understand the natural history of the NAION. The follow up studies on OCTA may help in understanding the natural history of NAION. Study of parafoveal vasculature by OCT-A explores the effect of NAION on macular vasculature, as well as further evaluates the possibility of a separate microvascular insult leading to macular thinning observed in NAION.

Fifteen eyes of 15 patients that presented with NAION presenting within < 6 weeks from symptom onset, were included in the study. Three patients could not follow up at 6 months owing to COVID-19 pandemic and hence were excluded from the analysis at 6 months. Fifteen age matched controls were also included in the study.

All patients and controls underwent SS-OCT-A on the Topcon Swept Source DRI OCT TritonTM and microvascular plexuses as segmented by the device were individually evaluated for longitudinal changes over the course of 6 months. To study differences at each plexus level, all scans were exported from the device and processed with imageJ software using Phansalkar algorithm (as described in methodology). ImageJ was preferred over automated software, as we can selectively eliminate the larger vessels in the scans which enables us to accurately measure the microvascular density, as reported by Dhiman et al9.

In the peripapillary scans, our study conclusively shows a significantly low microvascular density at all levels studied (superficial (ONH), radial peripapillary capillary, choriocapillaris) at presentation when compared to control group. The reduction in peripapillary retinal microvasculature in NAION, as noted by us, replicates the findings of previous studies3-9. The RPC layer, as described by Michaelson16 and Henkind17, is derived primarily from parapapillary retinal arterioles and forms a network within the RNFL layer that runs parallel to the axons and acts as the primary supply to the axons. As reported from few studies18,19, central retinal vasculature is not the sole contributor to the RPC layer and short posterior ciliary arteries do contribute via anastomosis.

As the primary insult in NAION is a transient hypoperfusion of posterior ciliary arteries, this may contribute to the RPC density reduction. In addition, a direct insult to the ONH in NAION results in axonal swelling, that sets up a cycle of compression of central retinal microvasculature that further contributes to ischaemia and resultant swelling. The choroidal filling defects are primarily seen in arteritic forms of AION, but they have been demonstrated in non-arteritic form also 20- 22. However, it should be noted in the acute setting where there is optic nerve head and RNFL edema, there is a high propensity for segmentation errors and loss of signal from underlying choriocapillaris that may lead to false low values .

On follow up of the study group, the peripapillary retinal microvasculature showed further drop in density. This reduction in microvasculature is likely a consequence of RNFL atrophy, that leads to a reduced metabolic demand and hence a rarefaction of the capillaries. At the level of peripapillary choriocapillaris, OCT-A revealed that the density returned to the level of controls and there was no significant difference between the two groups at 3 months and 6 months of follow-up. As mentioned previously, the initial transient reduction in choriocapillaris density followed by resurgence to normal levels could be a consequence of transient hypoperfusion in acute cases or simply an artifact of loss of underlying signal due to ONH oedema.

The assessment of microvasculature at the macula was done at superficial macular capillary plexus (SMD) and deep macular capillary plexus (DMD) and choriocapillaris (MCC). We found significant reduction in the SMD at presentation, from the control group. However there was no significant change seen in the microvascular density at superficial level at 3 months and 6 months. At the level of deep plexus, the microvascular density was significantly reduced when compared to controls. This also did not show any significant change over the course of 6 months.

The reduction in retinal microvasculature in NAION may seem counter-intuitive, considering that posterior ciliary arteries, which are the primary site of hypoperfusion in NAAION do not contribute to superficial and deep macular plexus. The secondary ganglion cell loss (GCC) that occurs in NAAION may represent the sole reason for reduced superficial density, as these capillaries nourish the GCC and reduces in response to reduced metabolic demand. In addition, there is a possibility that swelling at ONH may compress retinal microvasculature leading to decreased density at both superficial and deep layers at the macula.

Fard MA et al23 and ZY Tao et al11 both found reduced density only at the superficial level, thus affirming that the macular vessel density loss is secondary to GCC atrophy; Augstburger et al10 found reduced density at both superficial and deep levels, hinting at the component of retinal ischemia also. At the level of macular choriocapillaris, no change was seen between the groups. As the alteration in choroidal flow occurs only in peripapillary choroid in NAAION, this was an expected finding and discards any role of choroidal vasculature disturbance in macula.

To conclude, our study shows a decrease in peripapillary retinal microvasculature in NAION, that reduces further over 6 months as neuronal atrophy sets in. Macular microvasculature shows conclusive reduction in early stages, that remains stable through 6 months; the changes are definite at superficial level but changes at deep macular plexus may require further studies with adequate matching for validation.

The major limitation of this study is small sample size. And the fact that in the acute phase of NA-AION, the segmentation at ONH is prone for error due to oedema that distorts the anatomy, leading to potential errors in measurement. Nonetheless the study demonstrate that OCT-A in NAION can be useful in detecting microvasculature alterations occurring in the ONH and macula.

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