Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Quantitative Choriocapillaris Perfusion Before and After Vitrectomy in Idiopathic Epiretinal Membrane by Optical Coherence Tomography Angiography

Yanping Yu, MD; Yufei Teng, PhD; Meng Gao, MD; Xinxin Liu, MD; Jinqiu Chen, MD; Wu Liu, MD, PhD

Abstract

BACKGROUND AND OBJECTIVES:

To compare choriocapillaris perfusion of the fovea between patients with idiopathic epiretinal membrane (iERM) and normal controls and determine whether surgery affects it.

PATIENTS AND METHODS:

Both eyes of 45 patients with iERM and 28 healthy subjects were scanned by optical coherence tomography angiography (OCTA) preoperatively, and 25 of the patients were scanned postoperatively. Central parameters measured included flow area and parafovea vessel density of the foveal choriocapillaris.

RESULTS:

Both parameters were significantly lower in eyes with iERM (both P < .001) compared with both the unaffected fellow eyes and the normal control eyes (both P < .001) preoperatively, and they increased as the result of surgery, although it did not reach statistical significance. However, the differences between both eyes of patients became insignificant after surgery (both P > .05).

CONCLUSIONS:

OCTA may provide quantitative information regarding choriocapillaris perfusion. iERM influences the foveal choriocapillaris perfusion, which is reversible by surgery.

[Ophthalmic Surg Lasers Imaging Retina. 2017;48:906–915.]

Abstract

BACKGROUND AND OBJECTIVES:

To compare choriocapillaris perfusion of the fovea between patients with idiopathic epiretinal membrane (iERM) and normal controls and determine whether surgery affects it.

PATIENTS AND METHODS:

Both eyes of 45 patients with iERM and 28 healthy subjects were scanned by optical coherence tomography angiography (OCTA) preoperatively, and 25 of the patients were scanned postoperatively. Central parameters measured included flow area and parafovea vessel density of the foveal choriocapillaris.

RESULTS:

Both parameters were significantly lower in eyes with iERM (both P < .001) compared with both the unaffected fellow eyes and the normal control eyes (both P < .001) preoperatively, and they increased as the result of surgery, although it did not reach statistical significance. However, the differences between both eyes of patients became insignificant after surgery (both P > .05).

CONCLUSIONS:

OCTA may provide quantitative information regarding choriocapillaris perfusion. iERM influences the foveal choriocapillaris perfusion, which is reversible by surgery.

[Ophthalmic Surg Lasers Imaging Retina. 2017;48:906–915.]

Introduction

An epiretinal membrane (ERM), also known as macular pucker or cellophane maculopathy, first described in 1865, is an avascular, fibrocellular membrane that proliferates on the inner surface of the retina.1,2 The most common presenting symptoms include decreased visual acuity and metamorphopsia,1 which seriously impair quality of life. Without clear pathogenesis of the disease, idiopathic epiretinal membrane (iERM) mainly occurs in patients older than 50 years of age.2,3 The prevalence of iERM varies from 1.02% to 7.3% based on studies conducted in different parts of China.4–7 Previous studies have attempted to identify iERM causes and found risk factors including diabetes, hypercholesterolemia, hypertension, and history of smoking, although there have been no consistent associations established.8

Since blood and oxygen supply completely depend on choriocapillaries in the fovea, several studies have focused on the relationship between choroid blood perfusion and the development of iERM lately, utilizing enhanced depth imaging optical coherence tomography (OCT) to analyze subfoveal choroidal thickness in eyes with iERM.9–12 However, results between the studies were not consistent with one another for absence of direct observation of blood perfusion. To speculate choroid blood perfusion by measuring choroidal thickness lacks scientific evidence; therefore, it is imprecise to investigate the relationship between choriocapillaris perfusion and the development of iERM by choroidal thickness.

OCT angiography (OCTA), with the split-spectrum amplitude-decorrelation angiography (SSADA) algorithm, can visualize vasculature using motion contrast. Stationary tissue produces a nearly constant reflection, whereas moving tissue generates signals changing over time, and the only mobile part in the retina and choroid is blood flow.13 This technology has been widely used for diabetic retinopathy,14–16 age-related macular degeneration (AMD),17–20 and macular telangiectasia type 2,21–23 showing that OCTA can provide detailed images and quantitative information with reliable sensitivity and specificity.

The purpose of this study is to investigate the parameters of the choriocapillaris perfusion in eyes with iERM, unaffected fellow eyes, and normal control eyes using OCTA with the SSADA algorithm and compare the results. Choriocapillaris perfusion parameters before and after vitrectomy in eyes with iERM were also compared.

Patients and Methods

Study Population

Seventy-one patients with iERM and 30 healthy subjects were selected from Beijing Tongren Eye Centre, Beijing Tongren Hospital, from January to August in 2015, enrolled according to the tenets of the Declaration of Helsinki after signing written informed consent forms in accordance with the institutional review board of Beijing Tongren Hospital, Capital Medical University. The diagnosis was based on spectral-domain OCT system (Cirrus; Carl Zeiss Meditec, Jena, Germany) and intraoperative observation.

All participants underwent eye examinations including measurements of best-corrected visual acuity (BCVA), intraocular pressure (IOP), axial length (AXL), color fundus photography and OCT. IOP was tested using noncontact tonometry (Full Auto Tonometer TX-F; Canon Canada, Quebec). AXL was measured using IOL Master biometry (Carl Zeiss Meditec, Jena, Germany). Color fundus photography was performed with a non-mydriatic fundus camera (Canon, Melville, NY).

Finally, 45 patients with iERM were recruited. Exclusion criteria included macular or retina hole (13 subjects), AMD (one subject), refractive error of more than −6.00 diopters (five subjects), AXL more than 26.00 mm (two subjects), or unstable eye fixation (five subjects). Twenty-eight of the 30 healthy subjects were recruited as the other two subjects had AXLs more than 26.00 mm, respectively. The inclusion criteria of the controls were: BCVA better than 0.9, IOP between 10 mm Hg to 21 mm Hg, and no ocular disease history (excepting mild ocular surface diseases such as conjunctivitis). Left eyes were included for analysis.

Data Acquisition

OCTA images were obtained with the spectral domain system RTVue-XR Avanti (version 2014.2.0.93; Optovue, Fremont, CA). This apparatus incorporates an infrared laser that shines on and is reflected by the tissue. It has an A-scan rate of 70,000 scans per second and a B-san frame rate of approximately 200 frames per second, using a light source with a bandwidth of 45 nm centered on 840 nm.14,24,25 Individual scans of layers of the retina and choroid are collected to be A-scans. A-scans are compiled into a B-scan. The SSADA algorithm compares the amplitude fluctuation of the reflected light between the consecutive B-scans at different locations so that the static tissue would have a low decorrelation value, whereas blood flow has a high decorrelation value. Then blood flow could be distinguished from static background tissue.15 Each subject in this study underwent two repeated B-scans at the same position of a 3 mm × 3 mm area of scanning, which was centered on the fovea.

In this study, we analyzed the layer of choriocapillaris referring a 30 μm thick layer from 30 μm to 60 μm beneath the upper boundary of RPE18,26 from the en face OCT angiogram. The choriocapillaris perfusion was quantified by parameters including flow area and parafovea vessel density. The flow area refers to a circular region centered on the fovea with a radius of 1.25 mm, calculated by the number of pixels over the threshold (Figure 1). Parafovea area refers to a circle with a radius of 1.25 mm except an area of fovea avascular zone (diameter 0.6 mm) in the center position.26,27,28 Parafovea vessel density is defined as the percentage of positive pixels in parafovea area and is calculated using the formula: Vessel density = V × dA/dA, where V is 1 when the OCTA value is above a background threshold and 0 otherwise (Figure 2). “A” refers to the scan area. The threshold has been tested in trial test for accuracy, stability, and specificity, and the same threshold was used for all images of eyes included in this study.

The flow area (highlighted yellow) was marked as a circle with a radius of 1.25 mm. Flow area in the healthy normal eye is shown as 4.451 mm2.

Figure 1.

The flow area (highlighted yellow) was marked as a circle with a radius of 1.25 mm. Flow area in the healthy normal eye is shown as 4.451 mm2.

Parafoveal area (highlighted yellow) refers to a region with a radius of 1.25 mm and a deduction of 0.3 mm. Parafoveal vessel density in this healthy control eye is shown as 94% (0.94).

Figure 2.

Parafoveal area (highlighted yellow) refers to a region with a radius of 1.25 mm and a deduction of 0.3 mm. Parafoveal vessel density in this healthy control eye is shown as 94% (0.94).

Statistical Analysis

All the statistical calculations were performed by SPSS version 22.0 (SPSS, Chicago, IL). Comparisons of flow area and parafovea vessel density both before and after surgery among the eyes with iERM, unaffected fellow eyes, and normal control eyes were calculated using Kruskal-Wallis test. Wilcoxon signed-rank test was performed to evaluate changes of the two parameters for the eyes with iERM and parafovea vessel density of the unaffected fellow eyes for pre- and postoperative and paired t test was conducted to calculate flow area for the unaffected fellow eyes. A P value of less than .05 was considered as statistically significant.

Results

A total of 45 patients of iERM (13 males and 32 females; age range: 20 years to 76 years; median age: 64 years) and 28 normal controls (10 males and 18 females; age range: 56 years to 70 years; median age: 60 years) were enrolled in this study. All of the eyes with iERM underwent pars plana vitrectomy and internal limiting membrane peeling by the same experienced surgeon, and 25 out of the 45 patients with iERM complied with a 1-month return. Ocular and systemic characteristics along with demography features of all the participants are presented in Table 1.

Table 1:
Systemic Characteristics of Patients With iERM and Controls

Systemic Characteristics of Patients With iERM and Controls

Ocular Characteristics of Patients With iERM and Controls

Ocular Characteristics of Patients With iERM and Controls

Preoperative Choriocapillaris Perfusion Between iERM Patients and Controls

As is shown in Table 2, before surgery, the flow area was 4.194 mm2 (3.665 mm2 – 4.437 mm2) in eyes with iERM (Figure 3), which was significantly smaller than in unaffected fellow eyes ([4.492 mm2 ± 0.261 mm2]; P < .001, Kruskal-Wallis test) and normal control eyes ([4.577 mm2 ± 0.153 mm2]; P < .001, Kruskal-Wallis test) (Figure 4), respectively. The difference between the unaffected fellow eyes and normal control eyes was not statistically significant (P = .765, Kruskal-Wallis test). Similarly, parafovea vessel density in eyes with iERM (0.855; 0.755 ± 0.910) (Figure 5) was significantly lower than unaffected fellow eyes (0.920; 0.880 – 0.953) (P < .001, Kruskal-Wallis test) (Figure 6) and normal control eyes (0.933 ± 0.031; P < .001, Kruskal-Wallis test). P value was 0.509 for comparison between fellow eyes and control eyes, which meant no statistical significance either.

Preoperative Choriocapillaris Perfusion Parameters of Patients With iERM and Controls

Table 2:

Preoperative Choriocapillaris Perfusion Parameters of Patients With iERM and Controls

Flow area of this eye with idiopathic epiretinal membrane is shown as 4.136 mm2.

Figure 3.

Flow area of this eye with idiopathic epiretinal membrane is shown as 4.136 mm2.

Flow area in the unaffected fellow eye is shown as 4.373 mm2.

Figure 4.

Flow area in the unaffected fellow eye is shown as 4.373 mm2.

Parafoveal vessel density in this eye with idiopathic epiretinal membrane is shown as 85% (0.85).

Figure 5.

Parafoveal vessel density in this eye with idiopathic epiretinal membrane is shown as 85% (0.85).

Parafoveal vessel density in the unaffected fellow eye is shown as 89% (0.89).

Figure 6.

Parafoveal vessel density in the unaffected fellow eye is shown as 89% (0.89).

Comparisons of Pre- and Postoperative Choriocapillaris Perfusion Between Eyes With iERM and Unaffected Fellow Eyes

One month after pars plana vitrectomy and internal limiting membrane peeling, 25 of the 45 patients with iERM underwent our examination again. As shown in Table 3, in both eyes with iERM and the unaffected fellow eyes, the two parameters increased from the preoperative period to the postoperative period. Flow area of eyes with iERM increased to 4.246 mm2 (3.874 mm2 – 4.424 mm2; P = .247, Kruskal-Wallis test) and parafovea vessel density increased to 0.880 mm2 (0.795 mm2 – 0.910 mm2; P = .281, Kruskal-Wallis test), which did not reach the level of statistical significance. Comparisons between the pre- and postoperative periods for the unaffected fellow eyes showed no statistical significance, either (P > .05, paired t test for flow area; P > .05, Kruskal-Wallis test for parafovea vessel density).

Choriocapillaris Perfusion Parameters Before and After Operation of Patients With iERM

Table 3:

Choriocapillaris Perfusion Parameters Before and After Operation of Patients With iERM

Postoperative Choriocapillaris Perfusion Between iERM Patients and Controls

Flow area was still smaller and parafovea vessel density was still lower in eyes with iERM than in unaffected fellow eyes and normal control eyes, respectively, as shown in Table 4. Differences between eyes with iERM and normal control eyes remained significant (P < .001 for both flow area and parafovea vessel density, Kruskal-Wallis test). However, differences between eyes with iERM and unaffected fellow eyes became insignificant after surgery (P = .066 for flow area; P = .089 for parafovea vessel density; Kruskal-Wallis test).

Postoperative Choriocapillaris Perfusion Parameters of Patients With iERM and Controls

Table 4:

Postoperative Choriocapillaris Perfusion Parameters of Patients With iERM and Controls

Discussion

Over time, many researchers have focused on the choroid of eyes with iERM, trying to investigate the connection between subfoveal choroidal thickness and the development of this disease. However, their results were inconsistent and, thus, inconclusive.9–12 Michalewska et al. found that mean subfoveal choroidal thickness did not differ between eyes with iERM and fellow eyes, and it decreased significantly 3 months after vitrectomy and internal limiting membrane peeling. They suggested that dilatation of choroidal vessels or choroidal vascular hyperpermeability may result in the thickening of the choroid, which may have induced the development of iERM. On the other hand, normalization of retinal thickness after surgery may also normalize choroidal thickness, which means iERM affects choriocapillaris tremendously.9 They believed that there was an association between the choriocapillaris and the development of iERM, but distinguishing cause and effect was still problematic. Fujiwara et al. observed 64 eyes with iERM and 40 eyes with macular hole (MH) before and after vitrectomy, showing that the subfoveal choroidal thickness did not change either before or after vitrectomy. However, they still considered that choriocapillaris perfusion may be different during the time of measurement, because there is no evidence indicated that choroidal thickness represents choriocapillaris perfusion accurately.10 Zabadani et al. found that choroidal thickness did not show any statistically significant differences among eyes with iERM, the unaffected fellow eyes, or the control eyes. Accordingly, they concluded that iERM was a disease caused by changes in the vitreous body and choroid did not seem to participate in the pathogenesis.11 Anh et al. measured choroidal thicknesses and found that choroidal thicknesses in all positions significantly increased 1 week after vitrectomy compared to baseline in the iERM group and was only statistically significant for inferior choroidal thicknesses in the MH group. They inferred that the difference between the two groups may have been partially explained by the effect of gas tamponade and staying upright positioning.12 These findings are neither consistent nor technically comparable because no evidence shows that choroidal thickness could precisely suggest choriocapillaris perfusion, not to mention the measurement errors of the choroidal thickness and different methods of study design.

OCTA provides direct image and blood perfusion parameters of the retina and choroid, and for that reason it is a promising technique to solve the problem mentioned above. A number of studies of retinal layers have shown positive results with this technique,15–17 whereas quantitative research on the choriocapillaris remains limited correspondingly. Agem et al.14 found that choriocapillaris perfusion density values of eyes with diabetic retinopathy were significantly lower compared with controls. Jia et al.18 measured the choroidal neovascularization (CNV) area and flow index in AMD cases, finding that higher flow was detected with larger CNVs. Additionally, inner choroidal flow reduced when compared with the control cases that allowed visualization of larger and deeper choroidal vessels. Wang et al. measured the density of the superficial retinal network, deep retinal network, and choriocapillaris in normal eyes by the same machine with the same version of software as ours, which found the density of the macular vascular networks decreased with older age and was independent of AXL and subfoveal choroidal thickness in healthy individuals.29 All the results above certify OCTA as a new method of quantitative measurement of both retina and choroid with high sensitivity and specificity.

Using OCTA, this study observed the choriocapillaris of eyes with iERM, the unaffected fellow eyes, and the normal control eyes before and after surgery. We detected that flow area and parafoveal vessel density were significantly lower in eyes with iERM compared with the other two groups preoperatively; all the parameters in eyes with iERM have a tendency to increase because of surgery, although they do not reach the level of statistical significance compared with preoperative situations; significant differences of both parameters between eyes with iERM and the unaffected fellow eyes disappear after surgery. Etiology of iERM is not clear, possibly due to vitreous macular traction and choriocapillaris perfusion alteration. According to our study, it is highly probable that the iERM pathological situation adversely affects the choriocapillaris perfusion of fovea. Because of the short follow-up, the parameters do not approach level of statistical significance, but the tendency supports the indication.

This is the first study measuring choriocapillaris perfusion of eyes with iERM by OCTA, quantitatively comparing choriocapillaris perfusion in eyes with iERM by flow area and parafoveal vessel density with the unaffected fellow eyes together with normal control eyes, as well as making comparisons between pre- and postoperative situations. It provides quantitative information of choriocapillaris perfusion in eyes with iERM so that we conclude it is iERM that influences the foveal choriocapillaris perfusion instead of changes of choriocapillaris perfusion affecting the development of ERM. There are some limitations, such as short time of follow-up and small numbers of postoperative samples, which would be avoided during further research.

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Preoperative Choriocapillaris Perfusion Parameters of Patients With iERM and Controls

P Value
iERM EyesFellow EyesControl EyesiERM Eyes vs. Fellow EyesiERM Eyes vs. Control EyesFellow Eyes vs. Control Eyes
Flow Area (mm2)4.194 (3.665 – 4.437)4.492 ± 0.2614.577 ± 0.153.000.000.765
Parafovea Vessel Density0.855 (0.755 – 0.910)0.920 (0.880 – 0.953)0.933 ± 0.031.000.000.509

Choriocapillaris Perfusion Parameters Before and After Operation of Patients With iERM

iERM EyesFellow Eyes
PreoperativePostoperativeP Value Pre- vs. PostoperativePreoperativePostoperativeP Value Pre- vs. Postoperative
Flow Area (mm2)4.194 (3.665 – 4.437)4.246 (3.874 – 4.424).2474.492 ± 0.2614.409 ± 0.252.727
Parafoveal Vessel Density0.855 (0.755 – 0.910)0.880 (0.795 – 0.910).2810.920 (0.880 – 0.953)0.900 ± 0.095.679

Postoperative Choriocapillaris Perfusion Parameters of Patients With iERM and Controls

P value
iERM EyesFellow EyesControl EyesiERM Eyes vs. Fellow EyesiERM Eyes vs. Control EyesFellow Eyes vs. Control Eyes
Flow area (mm2)4.246 (3.874 – 4.424)4.409 ± 0.2524.577 ± 0.153.066.000.069
Parafoveal Vessel Density0.880 (0.795 – 0.910)0.900 ± 0.0950.933 ± 0.031.089.000.076
Authors

From Beijing Tongren Eye Center, Beijing Tongren Hospital, Beijing Ophthalmology and Visual Sciences Key Laboratory, Capital Medical University, Beijing (YY, YT, MG, JC, WL); Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing (YT); and the Department of Ophthalmology, Kailuan General Hospital, Hebei United University, Tangshan, China (XL).

Presented at the 21st Congress of Chinese Ophthalmological Society in China on September 11, 2016.

The authors report no relevant financial disclosures.

Address correspondence to Wu Liu, MD, PhD, Beijing Tongren Hospital, Capital Medical University, No 1, Dongjiaominxiang, DongCheng district, Beijing, China 100730; email: wuliubj@sina.com.

Received: February 19, 2017
Accepted: June 15, 2017

10.3928/23258160-20171030-06

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