|Year : 2019 | Volume
| Issue : 2 | Page : 43-51
Macular microvaculature evaluation using optical coherence tomography angiography in patients with high myopia
Walaa M. Elsherif, M. Tarek A. Moustafa, Heba R. Attaallah, Rabei M. Hassanien
Department of Ophthalmology, Faculty of Medicine, Minia University, Minya, Egypt
|Date of Submission||12-Nov-2019|
|Date of Acceptance||05-Dec-2019|
|Date of Web Publication||19-Feb-2020|
Dr. M. Tarek A. Moustafa
Department of Ophthalmology, Faculty of Medicine, Minia University, Minya
Source of Support: None, Conflict of Interest: None
Background: Myopia is one of the common refractive error. Optical Coherence Tomography Angiography (OCTA) is a non-invasive investigation of microvasculature of the retina. Aim: To evaluate the OCTA study of the FAZ area and vascular density (VD) at superficial capillary plexus (SCP), deep capillary plexus (DCP) and choriocapillaris (CC) in myopic patients versus healthy controls and their correlations to axial length (AL), best corrected visual acuity (BCVA) and spherical equivalent (SE). Setting and Design: Prospective cross-sectional comparative study. Methods and material 75 eyes of 54 patients, group A are 50 eyes with high myopia and group B are 25 eyes of age matched healthy controls. OCTA images were obtained, analyzed and compared using SPSS v.12 in both groups. Results: Foveal thickness was significantly increased in the myopic group (259.7±23.9) P=0.025, while the paravfoveal thickness was decreased (305.9±18.5) P < 0.001. Both superficial and deep FAZ area were increased in group A. The foveal VD at SCP was significantly higher in Group A (30.3±5.2) P=0.006. The whole image DCP VD was significantly lower (44.5±5.4) P < 0.001. Regarding CC, there was a significant difference in both foveal and parafoveal VD (66.1±4.9) (66.5±4.6) P=0.006 and 0.017, respectively, with both being higher in group A. The study also showed the importance of the CD at DCP and CC being negatively correlated with LogMAR BCVA and positively with the SE, while foveal thickness was positively correlated with the AL. Conclusion: OCTA is a valid and fast technique that could give insights about microvascular changes in myopia.
Keywords: Myopia, optical coherence tomography, optical coherence tomography angiography
|How to cite this article:|
Elsherif WM, Moustafa MT, Attaallah HR, Hassanien RM. Macular microvaculature evaluation using optical coherence tomography angiography in patients with high myopia. Egypt Retina J 2019;6:43-51
|How to cite this URL:|
Elsherif WM, Moustafa MT, Attaallah HR, Hassanien RM. Macular microvaculature evaluation using optical coherence tomography angiography in patients with high myopia. Egypt Retina J [serial online] 2019 [cited 2020 Apr 7];6:43-51. Available from: http://www.egyptretinaj.com/text.asp?2019/6/2/43/278676
| Introduction|| |
Myopia is one of the refractive errors that is commonly seen around the world. Individuals with high myopia are those with an abnormally long axial length (AL) exceeding a certain measure, (typically ≥25.5 or 26.50 mm), a refractive error of at least −5.0 diopter (D), and who exhibit characteristic pathological features.
Highly myopic eyes are at risk of vascular lesions such as submacular hemorrhage, choroidal neovascularization membrane (CNVM) and myopic foveoschisis leading to severe visual impairment., Early diagnosis would help in preventing these devastating complications.
Optical coherence tomography (OCT) is a noninvasive imaging modality whose ability to image intraocular structures in vivo has made it useful for detection and quantification of macular pathologies. Recently, noninvasive three-dimensional analysis of the macular microcirculation has become possible using OCT-based angiography protocols. OCT angiography (OCTA) uses the theory of motion contrast imaging to allow for high-resolution blood flow analysis and generate depth-resolved angiographic images in just a few seconds. An automated software has been developed to perform layer segmentation making analysis of the individual intraretinal layer thicknesses easier.,,,
In the past few years, many studies demonstrated the reliability and reproducibility of OCT and OCTA evaluation of macular thickness and microvasculature in healthy and myopic eyes.,,,, Previous studies showed retinal vascular alterations in myopes when compared to healthy controls.,,,,,,, There is a limited number of publications on the vasculature structure–function relationship.,,,
The aim of this study was to evaluate the microvasculature at the macular area in myopic eyes as compared to age-matched healthy controls using OCTA, as well as correlating these results to the AL, best corrected visual acuity (BCVA) and spherical equivalent (SE).
| Materials and Methods|| |
The study was approved by the local ethical committee. Written consents were signed by all the study population to the use of their data. The study adhered to the tenets of the Declaration of Helsinki.
This is a cross-sectional, prospective, case–control study. All study population were evaluated at a tertiary ophthalmology outpatient clinic facility in the period between March 2017 and December 2018. A total of 75 eyes of 54 patients were divided into two group; Group A included patients with high myopia, and Group B included the right eyes of age-matched healthy controls.
Inclusion criteria of patients in Group A were age between 18 and 45 years, highly myopic subjects defined as those with SEs of −6 D or more, with AL > 25.5 mm. Group B individuals were chosen among healthy age-matched controls. Any patients with myopic macular pathology (e.g., macular hole, epiretinal membranes, foveoschisis or CNVM) were excluded from the study. Glaucomatous patients or patients with history of intraocular surgery, intravitreal injection or retinal vascular diseases (e.g., diabetic retinopathy or hypertensive retinopathy) were also excluded. We also excluded captured images with the following criteria: low signal strength index (<50), media opacity obscuring the view, any presence of segmentation errors, presence of blink artifacts or poor fixation leading to motion or doubling artifacts.
All patients were asked to provide a detailed medical history. Meticulous ophthalmologic examination included refraction, BCVA measurement using Landolt C chart, intraocular pressure measurement using Goldman applanation tonometry, slit-lamp examination, AL measurement using AB and pachymetry scans (compact touch, Quantel Medical, Bozeman, MT, USA). Structural macular OCT and OCTA were also obtained using OptoVue machine (Avanti RTVue-XR; Optovue, Fremont, CA, USA).
Optical coherence tomography angiography image acquisition
The scans that was used were; retina map, which allowed us to determine the central macular thickness and parafoveal thickness (PFT), radial lines to exclude any associated retinal pathology such as diabetic retinopathy or CNVM; angio retina, with a scan area of 6 mm × 6 mm to detect the vessel density (VD) at the level ofsuperficial capillary plexus and deep capillary plexus (SCP and DCP) and choriocapillaris (CC), and the foveal avascular zone (FAZ) area at the level of SCP and DCP; and 3D widefield scan for retina map registration. The software used was the AngioAnalytics (RTVueXR version: 2017.1.0.151, Optovue, Inc., Fermont, California, USA).
Vessel density and foveal avascular zone measurement
AngioAnalytics are quantification tools that enable measurement of vessel area density, and nonflow area to measure the size of the FAZ. VD map was used to measure and compare the relative density of the flow, at the level of the SCP, DCP and CC, as a percentage of the total area. The VD is calculated as the percentage area occupied by the flowing vessels. [Figure 1] shows an example of the printout of OCTA image at the level of SCP of a patient from group A in comparison with a normal subject from Group B [Figure 1].
|Figure 1: Optical coherence tomography angiography printout of the left eye of a myopic patient (a) and the right eye of a normal subject (b) at the superficial capillary plexus level. Top left: An en face optical coherence tomography angiography slab at the superficial capillary plexus level. Top middle: An en face optical coherence tomography at the superficial capillary plexus level. Top right: Top table showing optical coherence tomography thickness (μm) of the 6 mm × 6 mm macular cube and vascular density (%) of the superficial capillary plexus of the whole image, fovea and parafovea. Bottom table showing grid-based vascular density (%) of the superficial capillary plexus. Bottom left: Structural B-scan optical coherence tomography of the macula with angio overlay. Bottom middle: Plain structural B-scan optical coherence tomography. Bottom right: Color-coded map showing vascular density at the superficial capillary plexus|
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AngioVue software (Optovue, Inc., Fermont, California, USA) assesses automatically the VD in a circle region of interest (ROI) with 2.5 mm in diameter, with its center on the center of the FAZ. The VD in the ROI is evaluated into two areas: A central circle with a diameter of 1 mm (foveal area [F]), and the remaining part inside the ROI is defined as parafoveal area (PF). The whole image VD is calculated as the density of the entire 6 × 6 area.
Using the acquired images, the FAZ area was measured in mm2 using the nonflow function on the OCTA software at the level of the superficial and deep retinal networks, [Figure 2] shows the en face OCTA slab at the level of the SCP in a myopic patient in comparison to a normal subject [Figure 2]. When the observer clicks on the center of the FAZ, the area of FAZ is automatically calculated by the software. OCTA images of the SCP and the DCP were automatically generated.
|Figure 2: An en face optical coherence tomography angiography slab at the level of the superficial capillary plexus in a myopic patient (a) and a normal control (b). The colored area represents the nonflow area of the foveal avascular zone at the level of superficial capillary plexus as automatically outlined by the AngioAnalytics software|
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Split-spectrum amplitude-decorrelation angiography or SSADA was used to extract the OCTA information. In order to minimize motion artifacts arising from micro-saccades and fixation changes, two orthogonal OCTA volumes were acquired.
BCVA was converted to logarithm minimum angle of resolution (LogMAR) for statistical purposes. Statistical analysis was performed using SPSS software V.21 (SPSS, Inc., Chicago, Illinois, USA). Analysis of quantitative data was performed using independent sample t-test and qualitative data using Chi-squared test. Data were displayed as range, mean ± standard deviation or frequency and percentage (%), P value was significant at < 0.05 level.
| Results|| |
The study included 75 eyes of 54 patients divided into two groups. Group A included 50 myopic eyes of 30 patients 18 males (60%) and 12 females (40%). The mean age was 33.9 ± 7.3 years (range 20–45 years) with a mean SE of −10.49 ± 2.86 D (range −6–−18 D). The mean AL was 27.6 ± 1.9 mm (range 25.5–33.8 mm) and the mean LogMAR BCVA was 0.26 ± 0.18 (range from 0 to 0.7). Group B included 25 normal right eyes of 25 patients 13 males (52%) and 12 females (48%). The mean age was 33.8 ± 4.9 years (range 24–42 years) with a mean SE of 0.07 ± 0.72 D (range 1.25–−1.25D). The mean AL was 22.7 ± 0.5 mm (range 22.1–23.5 mm) and the mean LogMAR BCVA was 0.05 ± 0.05 (range from 0 to −0.15).
There was no statistically significant difference between the two groups in age and sex. Whereas, there was significant difference in SE (P < 0.001), AL (P < 0.001), and LogMAR BCVA (P < 0.001) between the two groups.
Demographic and clinical characteristics of the studied individuals are shown in [Table 1] and [Table 2].
Each group was studied for seven parameters: foveal thickness, PFT, superficial FAZ, deep FAZ, SCP, DCP, and CC.
Central foveal thickness
The central foveal thickness (CFT) was significantly increased in the myopic group (259.7 ± 23.9 μm) compared to the control group (246.8 ± 21) (P = 0.025) [Figure 3]A.
|Figure 3: Column chart comparing foveal (A) and parafoveal (B) thicknesses between normal subjects and myopic patients|
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The PFT was significantly decreased in Group A when compared to Group B (305.9 ± 18.5 and 321.9 ± 13.4 μm, P < 0.001, respectively) [Figure 3]B.
Superficial foveal avascular zone area
Mean FAZ area at the level of SCP was significantly greater in Group A compared to Group B, (0.35 ± 0.08, 0.28 ± 0.06 mm2, P= 0.001, respectively) [Figure 4]A.
|Figure 4: Column chart comparing the area of superficial foveal avascular zones (FAZ) area (A) and the deep FAZ are (B) between normal subjects and myopic patients|
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Deep foveal avascular zone area
Mean FAZ area at the level of DCP was significantly greater in group A compared to group B, (0.45 ± 0.09, 0.33 ± 0.06 mm2, P < 0.001, respectively) [Figure 4]B.
The superficial capillary plexus
The whole image VD in the SCP was significantly lower in myopic eyes (43.9 ± 3.1) compared to normal group (48.9 ± 3.8) P < 0.001. On the other hand, foveal VD was significantly higher in myopic eyes (30.3 ± 5.2) P= 0.006, and there was no significant difference in parafoveal VD between both groups, these results are shown in [Table 3] and [Figure 5].
|Table 3: Comparison between the two groups regarding vessel density at the level of Superficial capillary plexus|
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|Figure 5: A column chart comparing whole image, foveal, and parafoveal vascular density at the level of the superficial capillary plexus between normal controls and myopic patients|
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The deep capillary plexus
The whole image DCP VD was significantly lower (44.5 ± 5.4) P < 0.001, the foveal DCP VD (27.7 ± 7.6) was significantly lower in myopic eyes P < 0.001, while no significant difference was found regarding parafoveal DCP VD. These results are shown in [Table 4] and [Figure 6].
|Table 4: Comparison between the two groups regarding vessel density at the level of the deep capillary plexus|
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|Figure 6: A column chart comparing whole image, foveal, and parafoveal vascular density at the level of the deep capillary plexus between normal controls and myopic patients|
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Regarding CC, the foveal and parafoveal VD were higher in the myopic eyes when compared to the normal ones, values were 66.1 ± 4.9; P= 0.006 and 66.5 ± 4.6; P= 0.017, respectively. However, there was not any significant difference between both groups regarding whole image VD. These results are shown in [Table 5] and [Figure 7].
|Table 5: Comparison between the two groups regarding vessel density at the level of choriocapillaris|
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|Figure 7: A column chart comparing whole image, foveal, and parafoveal vascular density at the level of the choriocapillaris between normal controls and myopic patients|
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In the present study we found positive correlation between LogMAR BCVA and deep FAZ area (P = 0.046) in the myopic group.
There was also a negative correlation between BCVA and each of deep whole image VD (P = 0.001), deep foveal VD (P = 0.047), deep parafoveal VD (P < 0.001) and CC whole image VD (P < 0.001). However, no significant correlation could be found between LogMAR BCVA and any of foveal thickness, PFT, superficial FAZ area, superficial whole image VD, superficial foveal VD, superficial parafoveal VD, and CC VD. Summary of BCVA correlations is shown in [Table 6] and [Figure 8]a [Figure 8]b [Figure 8]c [Figure 8]d [Figure 8]e.
|Table 6: Correlations between logarithm minimum angle of resolution best corrected visual acuity and all the parameters understudy (n=50)|
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|Figure 8: Scatterplot chart showing correlation between logarithm minimum angle of resolution best-corrected visual acuity and the vascular density at; deep foveal avascular zone area (a), deep whole image (b), deep fovea (c), deep parafovea (d), and choriocapillaris parafovea (e)|
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In the correlation done regarding the AL [Figure 9], there was positive correlation between foveal thickness and AL (P = 0.034). A negative correlation was also found between AL and superficial parafoveal VD (P = 0.002). No correlation could be found between AL and all other parameters. Summary of BCVA correlations is shown in [Table 7].
|Figure 9: Scatterplot chart showing correlation between axial length with foveal thickness (a) and superficial parafoveal vascular density (b)|
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|Table 7: Correlations between the axial length and all the parameters under study (n=50)|
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Correlation analysis between the SE and the previous parameters revealed a positive correlation regarding deep whole image VD (P = 0.003), deep foveal VD (P = 0.015), deep parafoveal VD (P < 0.001) and CC whole image VD (P = 0.009) [Figure 10]a [Figure 10]b [Figure 10]c [Figure 10]d. Summary of BCVA correlations is shown in [Table 8].
|Figure 10: Scatterplot chart showing correlation between spherical equivalent and vascular density at; deep whole (a), deep fovea (b), deep parafovea (c), and choriocapillaris whole image (d)|
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|Table 8: Correlations between spherical equivalent and all the parameters under study (n=50)|
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| Discussion|| |
Increased foveal thickness was significant in our study when compared to the age-matched healthy controls. Several studies showed the same results we noticed; Zhao et al. showed an increase in the foveal thickness with increased myopia. These findings were consistent with Luo et al., according to their work they found increased foveal thickness in myopic school children. Many explanations were given for this finding, one of them was the presence of tangential traction by the internal limiting membrane or posterior vitreous cortex,, but this reason was not the case in our study as we excluded any patient with retinal pathology. High permeability was suggested by Luo et al. to be the cause of increased foveal thickness., Another hypothesis by Sugimoto et al. was that the lack of large blood vessels and optic fibers at the peripheral retina makes it thinner than the central retina, which in turn makes the peripheral retina less resistant to traction and stretch. The preserved central retinal thickness is a compensation to the stretch over the entire retina. Another explanation of increased CFT is the associated choroidal dysfunctions in patients with high myopia, which could lead to photoreceptor apoptosis. The subsequent renewal of photoreceptors may cause elongation of the center outer segment layers.
In the present study, AL was positively correlated with the foveal thickness. Regarding the degree of myopia, there was a negative correlation between the SE and the foveal thickness.
Both the superficial and the deep FAZ areas were significantly larger in the high myopia group (0.35 ± 0.08 and 0.45 ± 0.09 mm2, respectively) in comparison to the normal group (0.28 ± 0.06 mm2 and 0.33 ± 0.06 mm2, respectively). This could be due to the decrease in VD in the myopic eyes. Tan et al. work showed that sex, central retinal thickness and SE influenced the superficial and deep FAZ areas in the myopic eyes. In separate analysis of high myopes, central choroidal thickness had a negative correlation with the superficial and deep FAZ size.
Decreased blood flow and perfusion of retinal vessels in myopic eyes have been reported in previous studies. Karczewicz and Modrzejewska found decreased blood flow when they used doppler ultrasonography in myopic patients. Zheng et al. investigated retinal vessel diameter in high myopia and found that both retinal arteriole and venule diameter were narrower than emmetropic eyes. Shimada et al. used laser blood flowmetry to study retinal blood flow, they reported reduced velocity in high myopia possibly due to narrow retinal vessel diameter. These findings, may indicate that there is no frank loss of retinal micro-vasculature and it is more due to decreased blood flow in the stretched micro-vessels.
In the current study, there was a significant decrease in whole image VD in the myopic group at the level of the superficial and DCPs, which is consistent with Al-Sheikh et al. and Fan et al. studies that were conducted on the same range of age and SE., Li et al. had the same exclusion criteria as our study with the same results of decreased capillary density at the level of both SCP and DCP of the highly myopic eyes. They studied high myopic eyes without retinopathy for VD and blood flow velocity (BFV), the latter showed no changes in the myopic eyes. It can be speculated that with the progressive elongation of AL and retinal tissue stretching, there is a decrease in retinal micro-vascular density.
Wang et al. also evaluated myopic eyes using OCTA and divided them into four groups; emmetropes, mild, moderate, and high myopes. In contrast to our study, there was no difference in the parafoveal VD at the SCP (P = 0.823) in the highly myopic group. This could be due to their small sample size as their study was conducted on only 18 high myopic eyes. Furthermore, the mean SE of their patients was only −8 D while in our study the mean SE was −10.49 D which permitted wider spectrum of severity of high myopia.
In our study, we found a negative correlation between LogMAR BCVA and the deep vascular layer VD (whole image, foveal and parafoveal), CC VD (whole image and parafoveal), and a positive correlation with both superficial and deep FAZ areas. Usui et al. assumed that two types of cells, horizontal and amacrine cells, were highly dependent on the DCP. They showed that the decrease of their density triggered profound effects on photoreceptor survival and function and hence VA. This could explain the inability to reach 6/6 vision in some of our high myopic patients included in the study.
AL and superficial parafoveal VD were negatively correlated to each other. It is possible that, in progressive myopia, some degeneration of the retinal pigment epithelium (RPE) cells and the retinal vascular endothelial cells happens due to stretched thinned retina resulting in decreased VEGF production and micro VD. Fan et al. found that, the longer the AL, the less VD was seen in the SCP and DCP at the macular area. However, they included highly myopic patients with retinal pathology.
In the work done by Wang et al., which was a population based survey on different refractive statuses, they found no correlation between the AL and the VD in the superficial and DCP using OCTA, even in highly myopic eyes, which may be attributed to the small sample size and the different study population (i.e., pediatric patients).
We also found a positive correlation between SE and deep plexus VD (whole image, foveal, parafoveal) and CC whole image VD. These results match with those of Fan et al. It means that the DCP and CC are more susceptible to the decrease in VD with increase of the myopia.
Segmentation errors are one of the most common artifacts in OCTA especially when obtaining images from high myopic eyes. Poor image quality is also seen with these patients due to the steep posterior segment curvature which is sometimes irregular. In the present study, the auto-segmented cuts were carefully reviewed and any images with segmentation errors or poor-quality signals were excluded.
To the best of our knowledge, our research is thefirst to include such detailed parameters in the study of the macular microvasculature, (foveal and PFT, superficial and deep FAZ areas, whole image, foveal and parafoveal VD at the level of SCP, DCP and CC), and their correlation with each of the AL, BCVA and degree of myopia.
On the other hand, we had some limitations in this study such as the relatively small sample size. Further longitudinal studies are required to establish the findings that are associated with progression.
| Conclusion|| |
We characterized the retinal microvasculature and microcirculation in high myopic eyes without retinopathy. The macular VD was decreased in both superficial and deep vascular plexuses and in the CC layer. These changes in VD are related to the AL and the SE, indicating that the globe elongation seen in high myopia could cause microvessel network stretch. The novel quantitative analysis of the retinal microvasculature may increase awareness to the underlying pathophysiology of myopia and enable prediction of visual function.
As the vision function is more related to the vasculature of deeper layers of the retina as well as the choroid, the more detailed and quantitative analysis of these layers could help in understanding of the pathophysiology and diagnosis of myopic retinopathy.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interes
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]