The Thickness of Each Retinal Layer and Visual Acuity after Vitrectomy in Idiopathic Epiretinal Membrane

Min Hwan Kim; Chan Yang Jeon; Seung Kook Baek; Young Suk Chang; Young Hoon Lee

doi:10.3341/jkos.2017.58.4.420

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Kim, Jeon, Baek, Chang, and Lee: The Thickness of Each Retinal Layer and Visual Acuity after Vitrectomy in Idiopathic Epiretinal Membrane

Original Article

J Korean Ophthalmol Soc 2017;58(4):420-429.

Published online: 8 September 2017

DOI: https://doi.org/10.3341/jkos.2017.58.4.420

The Thickness of Each Retinal Layer and Visual Acuity after Vitrectomy in Idiopathic Epiretinal Membrane

Min Hwan Kim, M.D.¹, Chan Yang Jeon, M.D.², Seung Kook Baek, M.D.³, Young Suk Chang, M.D.¹, Young Hoon Lee, M.D.^1,

^¹Department of Ophthalmology, Konyang University College of Medicine, Daejeon, Korea

^²Eyelove Clinic, Daejeon, Korea

^³Hwasun Country Public Health Center, Hwasun, Korea

Address reprint requests to Young Hoon Lee, MD Department of Ophthalmology, Konyang University Hospital, #158 Gwanjeodong-ro, Seo-gu, Daejeon 35365, Korea Tel: 82-42-600-9258, Fax: 82-42-600-9251 E-mail: astrix001@gmail.com

Received 20 October 20161 February 2017 Accepted 18 March 2017

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Purpose

In this study, we evaluated the thickness of each retinal layer using spectral-domain optical coherence tomography (OCT) and investigated the correlation between the thickness of each retinal layer and postoperative visual acuity in eyes with idiopathic epiretinal membrane (ERM).

Methods

his retrospective study included 46 eyes from 46 patients with idiopathic ERM who underwent pars plana vitrectomy. Each retinal layer thickness was measured by spectral-domain OCT before operation and at 1, 3, and 6 months after operation. The thickness of each retinal layer was evaluated in the control group before the operation. We performed an analysis of the changes in thickness of each retinal layer at 6 months after operation and then investigated the correlation between the retinal layer thickness and visual improvement.

Results

Preoperatively, the thickness of the retinal nerve fiber layer (RNFL) in the ERM group showed more increased compared with that in the control group, and the thickness of photoreceptors and retinal pigment epithelium were decreased compared to those in the control group. At 6 months after the operation, thickness changes were reduced at the RNFL, ganglion cell layer (GCL), inner plexiform layer (IPL), GCL-IPL complex, and outer plexiform layer, while the photoreceptor layer increased compared with the values preoperatively. Differences in the preoperative thickness of GCL between the two groups had a significant correlation with postoperative visual acuity (r = 0.477, p = 0.008).

Conclusions

Differences in preoperative thickness of the GCL between the two groups had a significant correlation with postoperative visual acuity. The greater was the thickness of the GCL, the worse was the visual outcome.

Keywords: Idiopathic epiretinal membrane, Pars plana vitrectomy, Retinal layer thickness, Visual acuity

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Figure 1.

Representative image of retinal layer division determined by the new segmentation application of the spectralis optical coherence tomography in epiretinal membrane (Segmentation Technology; Heidelberg Engineering, Inc., Heidelberg, Germany). 10 layers: 1 = inner limiting membrane, 2 = retinal nerve fiber layer, 3 = ganglion cell layer, 4 = inner plexiform layer, 5 = inner nuclear layer, 6 = outer plexiform layer, 7 = external limiting membrane, 8 = photoreceptor, 9 = retinal pigment epithelium, 10 = Bruch's membrane.

Figure 2.

Early Treatment of Diabetic Retinopathy Study (ETDRS) subfield. Central circle: fovea (F). Inner ring: superior inner (SI) + nasal inner (NI) + inferior inner (II) + temporal inner (TI). Outer ring: superior outer (SO) + nasal outer (NO) + inferior outer (IO) + temporal outer (TO). ETDRS subfields within standard 1-, 3-, and 6-mm-diameter concentric circles at the right used for reporting retinal thickness.

Figure 3.

Longitudinal changes of the average foveal thick-ness of each retinal layer before and after epiretinal membrane surgery. RNFL =retinal nerve fiber layer; GCL =ganglion cell layer; IPL =inner plexiform layer; INL =inner nuclear layer; OPL =outer plexiform layer; ONL =outer nuclear lay-er; PRL = photoreceptor; RPE = retinal pigment epithelium.

Table 1.

Demographic characteristics and clinical features of the patients

Characteristics	Value
Patients	46
Gender (male:female)	24:22
Age (years)	68.30 ± 11.13
Preoperative lens state (phakic:pseudophakic)	16:30
Phacovitrectomy: Vitrectomy	16:30
BCVA (logMAR) (preoperative:postoperative)	0.49 ± 0.36:0.26 ± 0.22^*
Complications and recurrence	0

Values are presented as mean ± SD unless otherwise indicated. SD = standard deviation; BCVA = best corrected visual acuity.

^* p-value < 0.05, Wilcoxon signed rank test.

Table 2.

Comparisons of the average retinal layer thickness in the preoperative epiretinal membrane (ERM) eye to the unaffected contralateral eye and average retinal thickness in the ERM eye before and after surgery

Variables	Preop	CE	p-value^*	Postop (6 months)	p-value^*
Fovea (μ m)	485.83 ± 86.30	274.03 ± 39.75	<0.001	389.90 ± 54.15	<0.001
Inner ring (μ m)	431.48 ± 59.72	330.44 ± 21.57	<0.001	363.74 ± 33.07	<0.001
Outer ring (μ m)	367.13 ± 42.45	307.27 ± 21.02	<0.001	318.78 ± 24.62	<0.001

Values are presented as mean ± SD unless otherwise indicated. SD = Standard deviation; Preop = preoperative; CE = Contralateral eye; Postop = postoperative.

^* Wilcoxon signed rank test.

Table 3.

Comparison between the average thickness of the each retinal layer in the preoperative epiretinal membrane (ERM) eye and the unaffected contralateral eye and changes of the each retinal layer thickness in the ERM eye at 6 months after surgery

Variables		ERM (Preop)	CE	p-value^*	Postop (6 months)	p-value^*
RNFL (μ m)	Fovea	85.23 ± 61.84	12.13 ± 2.52	<0.001	30.10 ± 30.17	<0.001
	IR	82.98 ± 43.84	27.00 ± 3.45	<0.001	37.31 ± 21.91	<0.001
	OR	67.94 ± 31.53	41.26 ± 2.52	<0.001	42.63 ± 13.35	<0.001
GCL (μ m)	Fovea	46.60 ± 12.00	19.76 ± 14.39	<0.001	41.43 ± 10.21	0.048
	IR	55.96 ± 9.36	52.68 ± 8.64	0.044	50.74 ± 8.73	0.017
	OR	41.90 ± 5.18	37.55 ± 3.77	0.024	35.15 ± 6.66	<0.001
IPL (μ m)	Fovea	45.70 ± 10.75	25.23 ± 10.78	<0.001	37.86 ± 9.60	0.009
	IR	50.85 ± 4.97	42.55 ± 5.68	0.002	41.72 ± 4.79	<0.001
	OR	38.49 ± 6.49	34.33 ± 4.30	<0.001	29.96 ± 4.82	<0.001
GCL-IPL complex	(μ m) Fovea	92.30 ± 20.91	43.76 ± 21.50	<0.001	79.30 ± 18.30	0.014
	IR	106.72 ± 13.20	97.87 ± 11.38	0.009	92.43 ± 12.78	<0.001
	OR	80.36 ± 10.19	74.65 ± 6.42	0.011	65.08 ± 11.21	<0.001
INL (μ m)	Fovea	47.93 ± 11.76	23.30 ± 9.61	<0.001	45.23 ± 11.72	0.399
	IR	48.62 ± 4.72	38.40 ± 3.51	<0.001	47.46 ± 6.08	0.934
	OR	43.17 ± 4.66	34.89 ± 3.79	<0.001	39.77 ± 5.15	<0.001
OPL (μ m)	Fovea	39.66 ± 8.58	26.36 ± 7.84	<0.001	36.23 ± 8.29	0.041
	IR	37.39 ± 4.35	34.44 ± 4.49	0.011	35.09 ± 3.90	0.045
	OR	32.94 ± 4.36	30.46 ± 5.80	0.013	29.49 ± 2.15	<0.001
ONL (μ m)	Fovea	109.73 ± 30.10	85.93 ± 15.45	0.001	102.10 ± 21.11	0.727
	IR	73.50 ± 11.93	64.44 ± 8.70	0.001	70.77 ± 11.88	0.162
	OR	64.17 ± 11.10	55.40 ± 8.22	0.001	61.64 ± 9.54	0.614
PRL (μ m)	Fovea	85.23 ± 5.15	89.10 ± 4.92	0.002	87.83 ± 5.57	0.019
	IR	80.69 ± 2.87	80.90 ± 2.90	0.475	82.51 ± 3.90	0.007
	OR	79.73 ± 3.50	78.40 ± 2.24	0.105	79.96 ± 3.41	0.249
RPE (μ m)	Fovea	16.00 ± 4.20	17.33 ± 3.15	0.017	16.50 ± 4.38	0.436
	IR	14.37 ± 1.72	15.20 ± 2.58	0.127	14.96 ± 2.58	0.186
	OR	13.97 ± 1.72	14.09 ± 2.50	0.228	13.67 ± 1.53	0.343

Values are presented as mean ± SD unless otherwise indicated. SD = Standard deviation; Preop = preoperative; CE = contralateral eye; Postop = postoperative; RNFL =retinal nerve fiber layer; IR = in-ner ring; OR = outer ring; GCL = ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL =outer plexiform layer; ONL =outer nuclear layer; PRL =photoreceptor layer; RPE = retinal pigment epithelium.

^* Wilcoxon signed rank test.

Table 4.

Interocular differences between the retinal thickness in the preoperative epiretinal membrane (ERM) eye and the unaffected contralateral eye according to the Early Treatment of Diabetic Retinopathy Study (ETDRS) subfield

Variables	CE	ERM	p-value^*
SI (μ m)	343.76 ± 17.62	458.60 ± 67.29	<0.001
II (μ m)	348.20 ± 36.96	446.43 ± 89.13	<0.001
NI (μ m)	342.00 ± 16.61	456.86 ± 73.01	<0.001
TI (μ m)	330.66 ± 22.98	458.53 ± 81.12	<0.001
SO (μ m)	303.33 ± 17.03	379.10 ± 58.48	<0.001
IO (μ m)	305.23 ± 51.51	351.83 ± 58.29	0.001
NO (μ m)	322.93 ± 19.45	375.60 ± 40.36	<0.001
TO (μ m)	297.46 ± 17.81	361.90 ± 59.26	<0.001

Values are presented as mean ± SD unless otherwise indicated.

SD = standard deviation; CE = contralateral eye; SI = superior inner; II = inferior inner; NI = nasal inner; TI = temporal inner; SO = superior outer; IO = inferior outer; NO = nasal outer; TO = temporal outer.

^* Wilcoxon signed rank test.

Table 5.

Changes of the average foveal thickness of each retinal layer before and after epiretinal membrane (ERM) surgery

Variables	Preop	1 month	3 months	6 months	p-value^*
CMT	485.83 ± 86.30	435.83 ± 64.06	403.20 ± 47.76	389.90 ± 54.15	<0.001
RNFL	85.23 ± 61.84	50.60 ± 48.84	37.60 ± 35.36	30.10 ± 30.17	<0.001
GCL	46.60 ± 12.00	45.23 ± 14.87	43.30 ± 11.29	41.43 ± 10.21	<0.001
IPL	45.70 ± 10.75	47.16 ± 13.01	39.73 ± 8.42	37.86 ± 9.60	<0.001
GCL-IPL complex	92.30 ± 20.91	95.06 ± 25.94	82.13 ± 18.13	79.30 ± 18.30	0.002
INL	47.93 ± 11.76	52.73 ± 10.69	49.90 ± 9.74	45.23 ± 11.72	0.072
OPL	39.66 ± 8.58	41.36 ± 10.45	37.03 ± 8.92	36.23 ± 8.29	0.043
ONL	109.73 ± 30.10	104.83 ± 21.74	109.10 ± 23.59	102.10 ± 21.11	0.212
PRL	85.23 ± 5.15	85.73 ± 5.00	87.80 ± 6.76	87.83 ± 5.57	0.009
RPE	16.00 ± 4.20	15.06 ± 2.34	16.50 ± 4.27	16.50 ± 4.38	0.520

Values are presented as mean ± SD unless otherwise indicated.

SD = standard deviation; Preop = preoperative; CMT = central macular thickness; RNFL = retinal nerve fiber layer; GCL = ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer; ONL = outer nuclear layer; PRL = photo-receptor layer; RPE = retinal pigment epithelium.

^* Friedman test.

Table 6.

Variables		ERM (Preop)	CE	p-value^*	Postop (6 months)	p-value^*
RNFL (μ m)	Fovea	72.45 ± 15.77	13.94 ± 3.59	<0.001	39.42 ± 22.45	<0.001
	IR	69.24 ± 5.94	26.68 ± 7.16	<0.001	35.54 ± 16.87	<0.001
	OR	54.16 ± 20.87	38.76 ± 8.74	<0.001	46.64 ± 16.71	<0.001
GCL (μ m)	Fovea	46.27 ± 21.73	22.10 ± 17.73	0.002	42.22 ± 22.04	0.046
	IR	52.36 ± 3.27	49.27 ± 7.02	<0.001	46.73 ± 3.22	0.024
	OR	40.02 ± 6.37	34.61 ± 7.14	0.034	36.14 ± 7.46	<0.001
IPL (μ m)	Fovea	46.60 ± 22.22	23.11 ± 3.61	0.009	37.20 ± 17.22	<0.001
	IR	53.46 ± 6.23	40.77 ± 7.16	<0.001	47.06 ± 13.27	0.019
	OR	46.30 ± 7.34	32.12 ± 6.64	0.017	33.22 ± 16.20	<0.001
GCL-IPL complex (μ m)	Fovea	92.24 ± 16.46	44.76 ± 16.34	<0.001	72.36 ± 12.62	<0.001
	IR	110.32 ± 17.10	97.62 ± 6.74	<0.001	76.72 ± 7.63	<0.001
	OR	77.32 ± 20.66	69.72 ± 3.00	<0.001	72.03 ± 2.27	0.054
INL (μ m)	Fovea	43.62 ± 12.73	25.70 ± 6.46	<0.001	41.22 ± 10.02	0.066
	IR	46.72 ± 6.06	32.72 ± 1.27	<0.001	40.27 ± 6.30	0.097
	OR	42.76 ± 6.21	36.73 ± 1.26	<0.001	37.61 ± 6.07	0.146
OPL (μ m)	Fovea	40.02 ± 2.46	27.76 ± 2.37	<0.001	37.22 ± 7.36	0.009
	IR	37.61 ± 4.27	36.73 ± 6.67	0.075	36.62 ± 1.73	0.223
	OR	32.07 ± 1.34	27.72 ± 2.37	0.013	27.27 ± 2.11	<0.001
ONL (μ m)	Fovea	102.00 ± 14.21	79.01 ± 14.73	<0.001	106.11 ± 13.46	0.106
	IR	77.22 ± 16.72	66.71 ± 6.02	<0.001	80.27 ± 10.21	0.146
	OR	67.67 ± 3.77	49.62 ± 7.07	<0.001	69.23 ± 3.76	0.227
PRL (μ m)	Fovea	86.21 ± 1.34	87.46 ± 6.72	0.541	89.02 ± 6.74	0.028
	IR	80.72 ± 7.71	79.62 ± 7.72	0.475	82.26 ± 7.72	0.030
	OR	77.62 ± 2.37	77.01 ± 2.77	0.105	77.27 ± 2.46	0.523
RPE (μ m)	Fovea	16.46 ± 2.20	16.91 ± 2.46	0.817	16.92 ± 1.17	0.327
	IR	14.20 ± 2.27	16.27 ± 2.72	0.127	14.51 ± 2.72	0.263
	OR	13.02 ± 2.14	14.27 ± 2.70	0.228	13.21 ± 1.32	0.463

Values are presented as mean ± SD unless otherwise indicated.

SD = Standard deviation; Preop = preoperative; CE = contralateral eye; Postop = postoperative; RNFL = retinal nerve fiber layer; IR = inner ring; OR = outer ring; GCL = ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer; ONL = outer nuclear layer; PRL = photoreceptor layer; RPE = retinal pigment epithelium.

^* Wilcoxon signed rank test.

Table 7.

Correlation between the visual prognosis and changes of retinal layer thickness in epiretinal membrane (ERM) eye and inter-ocular difference of retinal layer thickness

Variables		Changes of retinal layer thickness		Interocular difference of retinal layer thickness
Variables		r	p-value^*	r	p-value^*
CMT	Fovea	0.520	0.003	0.019	0.921
	IR	0.344	0.063	0.028	0.882
	OR	0.321	0.084	0.088	0.644
RNFL	Fovea	0.019	0.922	0.022	0.907
	IR	0.116	0.543	0.026	0.891
	OR	0.001	0.996	0.086	0.652
GCL	Fovea	0.157	0.408	0.477	0.008
	IR	0.120	0.528	0.014	0.940
	OR	0.095	0.619	0.341	0.065
IPL	Fovea	0.067	0.726	0.050	0.794
	IR	0.162	0.393	0.024	0.898
	OR	0.052	0.785	0.101	0.594
GCL-IPL complex	Fovea	0.102	0.592	0.132	0.487
	IR	0.054	0.779	0.083	0.662
	OR	0.084	0.660	0.021	0.910
INL	Fovea	0.026	0.892	0.087	0.649
	IR	0.026	0.891	0.260	0.116
	OR	0.018	0.926	0.247	0.188
OPL	Fovea	0.104	0.584	0.001	0.997
	IR	0.240	0.202	0.040	0.833
	OR	0.290	0.120	0.189	0.317
ONL	Fovea	0.005	0.980	0.030	0.874
	IR	0.311	0.094	0.034	0.859
	OR	0.347	0.060	0.168	0.374
PRL	Fovea	-0.054	0.776	-0.178	0.347
	IR	-0.221	0.240	-0.184	0.330
	OR	-0.185	0.327	0.161	0.394
RPE	Fovea	-0.005	0.971	-0.265	0.157
	IR	-0.265	0.157	-0.057	0.766
	OR	0.075	0.585	-0.166	0.381

CMT = central macular thickness; IR = inner ring; OR = outer ring; RNFL = retinal nerve fiber layer; GCL = ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer; ONL = outer nuclear layer; PRL = photoreceptor layer; RPE = retinal pigment epithelium.

^* Spearman correlation test.

Table 8.

Multivariate linear regression analysis of variables associated with visual prognosis

Variables	β ± SD	p-value
Age	0.005 ± 0.003	0.110
Sex	0.083 ± 0.066	0.223
Changes of retinal layer thickness
CMT (fovea)	0.002 ± 0.003	0.064
Interocular difference of retinal layer thickness
GCL (fovea)	0.005 ± 0.002	0.012

Values are presented as mean ± SD unless otherwise indicated. Overall R² = 0.707.

SD = standard deviation; CMT = central macular thickness; GCL =ganglion cell layer.

Table 9.

Correlation between the visual prognosis and changes of retinal layer thickness in epiretinal membrane (ERM) eye and in-terocular difference of retinal layer thickness on pseudophakic eyes

Variables		Changes of retinal layer thickness		Interocular difference of retinal layer thickness
Variables		r	p-value^*	r	p-value^*
CMT	Fovea	0.413	0.002	0.015	0.733
	IR	0.273	0.058	0.022	0.702
	OR	0.255	0.066	0.070	0.512
RNFL	Fovea	0.016	0.822	0.019	0.809
	IR	0.103	0.484	0.023	0.794
	OR	0.001	0.888	0.076	0.581
GCL	Fovea	0.175	0.455	0.532	0.009
	IR	0.134	0.589	0.015	0.989
	OR	0.106	0.691	0.380	0.072
IPL	Fovea	0.059	0.647	0.044	0.708
	IR	0.144	0.350	0.026	0.993
	OR	0.046	0.700	0.112	0.663
GCL-IPL complex	Fovea	0.090	0.528	0.117	0.543
	IR	0.048	0.870	0.074	0.739
	OR	0.093	0.588	0.274	0.855
INL	Fovea	0.032	0.709	0.008	0.067
	IR	0.028	0.886	0.323	0.114
	OR	0.001	0.921	0.220	0.209
OPL	Fovea	0.092	0.652	0.002	0.889
	IR	0.214	0.225	0.044	0.743
	OR	0.258	0.134	0.168	0.354
ONL	Fovea	0.006	0.875	0.026	0.976
	IR	0.347	0.083	0.030	0.959
	OR	0.309	0.067	0.187	0.333
PRL	Fovea	-0.048	0.866	-0.158	0.387
	IR	-0.197	0.268	-0.201	0.368
	OR	-0.206	0.365	0.143	0.391
RPE	Fovea	-0.006	0.866	-0.236	0.175
	IR	-0.236	0.175	-0.063	0.683
	OR	0.066	0.653	-0.148	0.425

^* Spearman correlation test.

Table 10.

Multivariate linear regression analysis of variables associated with visual prognosis on pseudophakic eyes

Variables	β ± SD	p-value
Age	0.006 ± 0.003	0.139
Sex	0.105 ± 0.083	0.285
Changes of retinal layer thickness
CMT (fovea)	0.002 ± 0.003	0.080
Interocular difference of retinal layer thickn	ness
GCL (fovea)	0.006 ± 0.002	0.015

Values are presented as mean ± SD unless otherwise indicated. Overall R² = 0.775.

SD = standard deviation; CMT = central macular thickness; GCL = ganglion cell layer.

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