1040-5488/14/9111-1328/0 VOL. 91, NO. 11, PP. 1328Y1334 OPTOMETRY AND VISION SCIENCE Copyright * 2014 American Academy of Optometry
ORIGINAL ARTICLE
Retinal Nerve Fiber Layer Configuration in Eyes with Epiretinal Membrane Jaeryung Oh*, Jong-Hyun Oh*, Jae Rock Do†, Minwook Chang*, and Choul Yong Park*
ABSTRACT Purpose. To characterize configurations of the optic nerve head (ONH) and peripapillary retinal nerve fiber layer (RNFL) eyes with epiretinal membrane (ERM). Methods. We reviewed medical records of consecutive patients with ERM who were examined between September 2012 and August 2013. Patients were categorized based on the severity of ERM on fundus imaging; patients with ERM but without retinal distortion were in group 1, and patients with ERM and retinal distortion were in group 2. Optic nerve head and RNFL parameters measured by spectral domain optical coherence tomography were assessed and compared between eyes with ERM and normal fellow eyes. Results. There were no significant differences in ONH and RNFL parameters between ERM eyes and normal fellow eyes in group 1 (n = 12). In group 2 (n = 33), cup volume was smaller (p = 0.020), temporal quadrant RNFL thickness was greater by 18.8 T 16.6 Km (p G 0.001), and RNFL peak angle was smaller by 18.7 T 25.3 degrees in ERM eyes compared with fellow eyes (p = 0.001). In the 15 patients in group 2 who underwent ERM removal, temporal quadrant RNFL thickness decreased and the RNFL peak angle increased after the surgery (p = 0.008 and p = 0.001, respectively). Conclusions. The configurations of the ONH and peripapillary RNFL in eyes with ERM were different from those in fellow eyes. The characteristic configurations of RNFL such as small peak angle and temporal quadrant thickening may be considered when evaluating parameters as measured by spectral domain optical coherence tomography. (Optom Vis Sci 2014;91:1328Y1334) Key Words: epiretinal membrane, optic nerve head, peripapillary retinal nerve fiber layer, spectral domain optical coherence tomography, glaucoma
M
acular epiretinal membrane (ERM) is an avascular, fibrocellular membrane that proliferates on the inner retinal surface and may lead to various degrees of visual impairment.1 Epiretinal membrane is a relatively common disease, with a prevalence of 7 to 11.8% in two large population studies.2,3 Mild forms are characterized by an abnormal retinal light reflex on fundoscopy with mild retinal thickening and no distortion of the retinal surface.4 However, in some patients, there may be progressive contraction of the ERM, resulting in distortion of the retinal surface.4,5 Although the diagnosis of an ERM is usually straightforward by fundus examination, optical coherence tomography (OCT) may be useful to diagnose ERM and to monitor the clinical course of ERMs before and after surgery.4,6Y9
*MD, PhD † MD Department of Ophthalmology, Korea University College of Medicine, Seoul, South Korea (JO); and Department of Ophthalmology, Dongguk University Ilsan Hospital, Goyang, South Korea (J-HO, JRD, MC, CYP).
In addition to the macular images, OCT can provide images of the optic nerve head (ONH) and the peripapillary retinal nerve fiber layer (RNFL). Using these images, OCT software programs automatically measure RNFL thickness at each pixel along the peripapillary circle. They also measure ONH parameters, including optic rim area, optic disc area, average cup/disc ratio, vertical cup/disc ratio, and optic cup volume.10 Chronic, progressive loss of RNFL tissue is the hallmark of glaucomatous optic neuropathy.11 The ONH is typically examined for signs of glaucomatous damage by assessing the status of the neuroretinal rim.12 Therefore, evaluation of the ONH and peripapillary RNFL using OCT is useful for the diagnosis and management of glaucoma.10,13Y15 However, previous studies reported that compounding conditions such as myopia, optic disc size, and corneal astigmatism may affect parameters of the RNFL and ONH as measured by OCT.16Y18 We hypothesized that configurations of the ONH and peripapillary RNFL could be different from those of fellow eyes. In the present study, we investigated the effect of ERM on
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al.
parameters of the ONH and the RNFL as measured by spectral domain (SD)-OCT.
METHODS This study was designed as a retrospective case series. We obtained institutional review board approval from the Dongguk University Ilsan Hospital in Goyang, South Korea. All research adhered to the tenets of the Declaration of Helsinki.
Patients and Data Collection We retrospectively reviewed the medical records of consecutive patients with macular ERM who were examined at Dongguk University Ilsan Hospital between September 2012 and August 2013. Epiretinal membrane was diagnosed by fundus examination and SD-OCT examination. Patients with high myopia (9j6 diopters), glaucoma, diabetic retinopathy, retinal vein occlusion, agerelated macular degeneration, or a history of uveitis were excluded from the study. Seventy Korean patients with idiopathic ERM were reviewed. Thirteen patients were excluded because of high myopia (three eyes), glaucoma (one eye), diabetic retinopathy (five eyes), retinal vein occlusion (one eye), age-related macular degeneration (two eyes), or a history of uveitis (one eye) in ERM eyes or fellow eyes. Twelve patients had bilateral ERM. In a total of 45 patients with unilateral ERM, ERM eyes were compared with normal fellow eyes. Epiretinal membrane removal was performed in 15 eyes from 15 patients. Of these, four eyes of four patients with bilateral ERM were included. All SD-OCT images had a signal-to-noise ratio of 0.7 or higher. Data including age, sex, best-corrected Snellen visual acuity, central subfield retinal thickness, ONH parameters, peripapillary RNFL parameters, and fundus photographic images were
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obtained. In 15 eyes that underwent ERM removal, postoperative data were also obtained. The decision to operate on the ERM was based on the patient’s macular symptoms. All surgeries were performed by a single surgeon (J-HO). A three-port 23-gauge transconjunctival sutureless vitrectomy was performed under general anesthesia using the Constellation Vision System (Alcon Laboratories, Inc, Fort Worth, TX) and the noncontact wide-angle viewing system (BIOM 3; Oculus, Wetzlar, Germany). In patients with a visually significant cataract, phacoemulsification with implantation of an intraocular lens was performed before vitrectomy. Posterior vitreous detachment was induced with active outcome suction over the optic disc if posterior vitreous detachment was not already present. Triamcinolone acetonide was used to assist visualization and removal of posterior hyaloid and ERM. After complete removal of the posterior vitreous and extensive shaving of the peripheral vitreous, the ERM was removed using end-gripping forceps. A contact lens (Hoya Corp, Tokyo, Japan) was used to view the macula. In the eight most recent cases, the internal limiting membrane (ILM) was also peeled using end-gripping forceps after indocyanine green staining.
OCT Imaging Spectral domain optical coherence tomography was performed using the Cirrus HD-OCT (Model 4000, software version 6.0, Carl Zeiss Meditec, Dublin, CA) using a wavelength of 840 nm and an axial resolution of 5 Km. All SD-OCT included a macular cube scan and an optic disc cube scan. The 512 by 128 macular cube scan produces 128 horizontal scan lines, composed of 512 A-scans per line over a 6- by 6-mm area. Central subfield retinal thickness is assessed at the macular center (1 mm diameter) using a topographic map of the macular cube scan. The 200 by 200 optic disc scan captures a 6 by 6-mm2 cube, which is formed from 200 A-scans for each of 200 B-scans. A circle 3.46 mm in diameter consisting
FIGURE 1. Measurements of the RNFL peak angle using a TSNIT curve of the Cirrus HD-OCT (left bottom). The median value of points that had the greatest RNFL thickness was determined in the superior (a) or inferior (b) side of the TSNIT curve. Then, the locations of the superior (>) and inferior (A) RNFL peak were calculated in the angular values by the following formulas: > (degrees) = a 360/256, A (degrees) = (256 j b) 360/256. The RNFL peak angle was calculated from the sum of superior and inferior peak locations. A color version of this figure is available online at www.optvissci.com. Optometry and Vision Science, Vol. 91, No. 11, November 2014
Copyright © American Academy of Optometry. Unauthorized reproduction of this article is prohibited.
1330 Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al.
of 256 A-scans is then automatically positioned around the optic disc. The RNFL thickness along this peripapillary circle is measured at each pixel and an RNFL thickness map is generated. Optic nerve head parameters including disc area, rim area, average cup/disc ratio, vertical cup/disc ratio, and cup volume are automatically measured.19 The disc margin is defined as the termination of the Bruch membrane. The rim width around the entire circumference of the optic disc is then determined by measuring the thickness of the neuroretinal tissue in the optic nerve as it turns to exit through the opening in the Bruch membrane. The average cup/disc ratio is calculated by taking the square root of the ratio of the cup area to the disc area. The vertical cup/disc ratio is the ratio of the cup diameter to the disc diameter in a vertical meridian through the cup center. The cup volume is a three-dimensional measurement defined as the volume between the vitreoretinal interface and a plane at a fixed offset located 200 Km from the plane of the optic disc.20 The location of superior or inferior RNFL peaks was evaluated on the RNFL temporal, superior, nasal, inferior, and temporal (TSNIT) curve of the Cirrus HD-OCT (Fig. 1).21 The median value of points with the greatest RNFL thickness was determined in the superior (a) or inferior (b) side of the TSNIT curve. The peak locations appeared as points ranging from 0 to 255, as provided by the Cirrus HD-OCT algorithm. Then, the locations of the superior (>) and inferior (A) RNFL peak were calculated in angular values by the following formulas: > (degrees) = a 360/256, A (degrees) = (256 j b) 360/256. The RNFL peak angle was calculated from the sum of superior and inferior peak locations.
statistics were two tailed, and a p value less than 0.05 was considered significant.
RESULTS OCT Parameters between Eyes with ERM and Fellow Eyes The mean (TSD) age of 45 patients with unilateral ERM was 64.1 (T8.1) years. Fifteen (33.3%) of the patients were male and 30 (66.7%) were female. Twenty-two (48.9%) of the affected eyes were right eyes and 23 (51.5%) were left eyes. Of 45 total ERM eyes, 12 (26.7%) eyes with grade 1 ERM were categorized into group 1; 28 (62.2%) eyes with grade 2 ERM and 5 (11.1%) eyes with grade 3 ERM were categorized into group 2. There were no significant differences in ONH parameters and peripapillary RNFL parameters between affected and unaffected eyes of patients in group 1 (Table 1). However, several parameters were significantly different between affected and unaffected eyes in group 2, as shown in Table 2. Epiretinal membrane eyes had smaller cup volume than fellow eyes (p = 0.020). The average RNFL thickness was 5.0 T 10.7 Km thicker in ERM eyes (p = 0.011). Although superior, inferior, and nasal quadrant RNFL TABLE 1.
Comparison of measurements between affected and unaffected eyes of patients in group 1 with ERM but no retinal distortion n = 12
ERM and OCT Parameters Epiretinal membrane severity on fundus imaging was graded based on the three-step scale used in previous studies.22Y24 Grade 1 represented visible membranes without retinal distortion, grade 2 membranes had mild-to-moderate macular striae or vessel straightening, and grade 3 membranes had moderate-to-severe striae with vascular straightening.22 Two independent observers (J-HO and JRD) graded ERM severity. If there was discordance, a third observer (CYP) decided the grade. We classified patients with grade 1 ERM within group 1 and patients with grade 2 or grade 3 ERM within group 2. Group 1 represented patients with ERM without retinal distortion, and group 2 represented patients who had ERM associated with retinal distortion. Optical coherence tomography parameters were compared between eyes with ERM and normal fellow eyes in groups 1 and 2. Several patients in group 2 underwent vitrectomy for the removal of ERM. In those cases, OCT parameters were also compared before and after the surgery.
Statistical Analyses All data were analyzed using SPSS software version 20.0 (SPSS Inc, Chicago, IL). Descriptive statistics included the mean, SD, and proportion, as appropriate. The Kolmogorov-Smirnov test was used to verify the normality of the distribution of continuous variables. For comparison between two groups, the paired t test or the Mann-Whitney U test was used for continuous variables and the Fisher exact test was used for categorical variables. All
BCVA, logMAR Snellen equivalent Central subfield retinal thickness, Km ONH parameters Rim area, mm2 Disc area, mm2 Average cup/disc ratio Vertical cup/disc ratio Cup volume, mm3 Peripapillary RNFL parameters Average thickness, Km Superior quadrant thickness, Km Inferior quadrant thickness, Km Temporal quadrant thickness, Km Nasal quadrant thickness, Km Peak angle, degrees Superior peak location, degrees Inferior peak location, degrees
ERM eyes
Fellow eyes
p
0.06 T 0.12 20/23 283.0 T 45.6
0.03 T 0.05 20/21 251.1 T 21.4
0.705
1.20 T 0.18 1.88 T 0.34 0.57 T 0.13 0.54 T 0.12 0.20 T 0.17
1.21 T 0.13 1.97 T 0.36 0.59 T 0.12 0.56 T 0.10 0.24 T 0.18
0.999 0.209 0.141 0.344 0.255
92.4 T 9.1 114.6 T 13.3
90.8 T 7.2 110.7 T 11.3
0.454 0.239
115.8 T 21.1
120.3 T 16.9
0.116
72.6 T 14.4
68.5 T 12.2
0.168
63.7 T 9.8
66.3 T 9.2
0.142
147.4 T 19.2 75.8 T 14.9
145.9 T 19.9 74.2 T 14.9
0.455 0.582
71.6 T 10.0
71.7 T 9.0
0.875
0.021
Results are expressed as mean T SD. p values were calculated with Wilcoxon signed rank test. BCVA, best-corrected visual acuity; logMAR, logarithm of the minimum angle of resolution.
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al. TABLE 2.
Comparison of measurements between affected and unaffected eyes of patients in group 2 with ERM and retinal distortion n = 33
ERM eyes
BCVA, logMAR Snellen equivalent Central subfield retinal thickness, Km ONH parameters Rim area, mm2 Disc area, mm2 Average cup/disc ratio Vertical cup/disc ratio Cup volume, mm3 Peripapillary RNFL parameters Average thickness, Km Superior quadrant thickness, Km Inferior quadrant thickness, Km Temporal quadrant thickness, Km Nasal quadrant thickness, Km Peak angle, degrees Superior peak location, degrees Inferior peak location, degrees
Fellow eyes
p
0.19 T 0.21 0.04 T 0.05 G0.001 20/31 20/22 363.4 T 101.4 244.7 T 18.6 G0.001
1.31 T 0.27 1.93 T 0.37 0.53 T 0.16 0.48 T 0.15 0.13 T 0.10
1.27 T 0.23 1.98 T 0.33 0.57 T 0.12 0.54 T 0.12 0.17 T 0.13
0.347 0.303 0.068 0.053 0.020
95.2 T 8.5 112.0 T 16.3
90.2 T 13.4 109.2 T 20.6
0.011 0.373
114.6 T 17.8
117.2 T 20.5
0.367
87.9 T 16.8
69.1 T 10.9 G0.001
66.2 T 8.9
65.4 T 13.6
130.1 T 22.9 63.6 T 15.6 66.5 T 15.7
0.710
148.8 T 20.5 G0.001 77.0 T 13.5 G0.001 71.9 T 12.9
0.066
Results are expressed as mean T SD. p values were calculated with paired t test. BCVA, best-corrected visual acuity; logMAR, logarithm of the minimum angle of resolution.
thickness did not differ between both eyes, temporal quadrant RNFL thickness was thicker in ERM eyes than in fellow eyes by 18.8 T 16.6 Km (p G 0.001). The RNFL peak angle was 18.7 T 25.3 degrees smaller in ERM eyes than in fellow eyes (p = 0.001). Although inferior RNFL peak location did not differ between affected and unaffected eyes, the superior RNFL peak location was significantly smaller in ERM eyes than in fellow eyes, a difference of 13.3 T 19.6 degrees (p G .001). Central subfield retinal thickness was significantly thicker in ERM eyes than in normal fellow eyes in both groups 1 and 2 (p = 0.021 and p G 0.001, respectively).
Before and after ERM Removal In 8 (53.3%) of 15 eyes that underwent ERM removal, ILM peeling was also performed. Twelve (80%) eyes underwent cataract surgery at the same time. Postoperative OCTs were performed 10.1 T 6.4 weeks (mean T SD) (range, 5 to 24 weeks) after the surgery. After the surgery, temporal quadrant RNFL thickness decreased and RNFL peak angle significantly increased (p = 0.008 and p = 0.001, respectively, Fig. 2). However, cup volume did not differ significantly between before and after surgery (p = 0.571). There were no significant differences in the decrease of temporal quadrant RNFL thickness or the increase of RNFL peak angle
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between groups with and without additional ILM peeling (p = 0.163 and p = 0.269, respectively).
DISCUSSION Evaluation of the ONH and peripapillary RNFL is fundamental for the diagnosis and management of glaucoma.10,13Y15 However, various factors can affect their morphology. Hwang et al.21 reported that the eyes with a myopic temporal optic disc tilt and counterclockwise rotation had a thicker temporal RNFL and a more temporally positioned superior peak location. In another study, they reported that vitreopapillary traction caused RNFL thickening.25 Other studies have reported that race, ethnicity, myopia, optic disc size, and corneal astigmatism affected parameters of the ONH and RNFL.16Y19,26Y28 In the present study, we showed that these parameters were also affected by ERM. Direct mechanical traction by a contractile ERM may affect the ONH and peripapillary RNFL beyond the macula.29 In addition, the shift of the RNFL peak toward the fovea may cause the thickened temporal quadrant RNFL.30 In the present study, the RNFL peak angle and the superior RNFL peak shifted toward to the fovea in eyes with ERM-associated retinal distortion compared with fellow eyes, although the location of the inferior RNFL peak did not differ significantly. The results of the current study suggest that the macular pathology should be evaluated in eyes with RNFL peaks shifted toward the fovea and greater temporal RNFL thickness compared with fellow eyes. Some patients have visual symptoms owing to severe ERM-related retinal distortion, and clinicians may recognize macular pathology with detailed history taking. However, other patients may have no visual symptoms even with ERM-related retinal distortion. In these cases, characteristic findings of the ONH and RNFL in eyes with ERM would be helpful in recognizing macular pathology. More advanced ERM has contractile components that exert traction on the underlying retina, distorting the retinal vasculature.4,31 In the present study, we hypothesized that contraction of the ERM may affect the ONH and peripapillary RNFL beyond the macula. Therefore, we categorized eyes with ERM into two groups based on the presence or absence of ERM-associated retinal distortion and evaluated the effect of ERM severity on parameters of the ONH and the peripapillary RNFL as measured by SDOCT. Although ONH and RNFL parameters were not affected in eyes with ERM without retinal distortion, smaller cup volume, greater temporal quadrant RNFL thickness, and smaller RNFL peak angle were observed in eyes with ERM-associated retinal distortion compared with normal fellow eyes. The results suggest that the clinicians may consider additional studies for evaluation of the ONH and RNFL in glaucomatous eyes with ERM and retinal distortion. In addition, ERM is known to be progressive. Progression from less severe ERM without retinal distortion to more severe ERM with retinal distortion was observed in 9% of patients after 5 years in an older Australian population.32 Although no parameters of the ONH and RNFL were affected in eyes with ERM without retinal distortion, those parameters may be affected if the ERM progresses to include retinal distortion. Therefore, clinicians should be aware that ERM progression may cause changes in ONH and RNFL parameters in glaucomatous eyes that have been associated with ERM without retinal distortion.
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1332 Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al.
FIGURE 2. Preoperative (right) and postoperative (left) fundus photographs and OCT images of an eye that underwent ERM removal. Six weeks after the surgery, temporal quadrant RNFL thickness decreased from 115 to 77 Km and RNFL peak angle increased from 115.3 to 136.4 degrees (bottom). A color version of this figure is available online at www.optvissci.com.
Reddy et al. investigated the change of RNFL thickness in ERM eyes that underwent vitrectomy.29 We also evaluated the effect of ERM surgery on these parameters and demonstrated that temporal quadrant RNFL thickness decreased and RNFL peak angle significantly increased after ERM removal. There is debate as to the potential benefit of completing an ILM peeling after ERM removal.4 In a previous study, ILM peeling was correlated with improved unfolding of the posterior pole in eyes operated on for ERM.33 Some surgeons may consider ILM peeling in eyes with ERM and severe retinal distortion. In the present study, however, additional ILM peeling did not affect restoration of the temporal quadrant RNFL thickness or RNFL peak angle. Further largescale studies are needed to confirm the effect of ILM peeling on
retinal topographic changes using RNFL parameters measured by SD-OCT. One major limitation of this study is the small number of cases. Inferior peak location did not differ statistically between eyes with ERM and retinal distortion and fellow eyes. The topographic location of ERM may affect this result. However, the limited number of cases prevented further analysis. Another limitation is that all patients did not routinely undergo examinations such as red-free fundus photography and a visual field test for glaucoma evaluation. However, they had a normal range of intraocular pressures and their optic discs did not appear glaucomatous. It is possible that segmentation errors in OCT software caused the thickened temporal quadrant RNFL in eyes with ERM and retinal distortion.
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Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al.
Retinal nerve fiber layer thickness measured by SD-OCT may include the thickness of the ERM at temporal quadrant.34 Asrani et al.34 demonstrated that ocular pathologic features were the most common cause of artifacts in RNFL scans and the primary ocular pathologic feature accounting for artifacts was the presence of an ERM. Direct mechanical traction by a contractile ERM may change the configuration of the ONH, resulting in smaller cup volume. However, other ONH parameters did not differ between eyes with ERM and fellow eyes, and cup volume did not differ significantly between before and after surgery. In conclusion, the configurations of the ONH and peripapillary RNFL in eyes with high-grade ERM were different from those in fellow eyes. The characteristic configurations of RNFL such as small peak angle and temporal quadrant thickening may be considered as a confounding factor when evaluating parameters as measured by SD-OCT.
ACKNOWLEDGMENTS This research was supported by a grant from the Korean Health Technology R&D Project, Ministry of Health and Welfare, Republic of Korea (HI10C1979). Received March 2, 2014; accepted June 30, 2014.
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Jong-Hyun Oh Department of Ophthalmology Dongguk University Ilsan Hospital 27, Dongguk-ro, Ilsandong-gu Goyang, 410-773 South Korea e-mail: [email protected]
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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ORIGINAL ARTICLE
Retinal Nerve Fiber Layer Configuration in Eyes with Epiretinal Membrane Jaeryung Oh*, Jong-Hyun Oh*, Jae Rock Do†, Minwook Chang*, and Choul Yong Park*
ABSTRACT Purpose. To characterize configurations of the optic nerve head (ONH) and peripapillary retinal nerve fiber layer (RNFL) eyes with epiretinal membrane (ERM). Methods. We reviewed medical records of consecutive patients with ERM who were examined between September 2012 and August 2013. Patients were categorized based on the severity of ERM on fundus imaging; patients with ERM but without retinal distortion were in group 1, and patients with ERM and retinal distortion were in group 2. Optic nerve head and RNFL parameters measured by spectral domain optical coherence tomography were assessed and compared between eyes with ERM and normal fellow eyes. Results. There were no significant differences in ONH and RNFL parameters between ERM eyes and normal fellow eyes in group 1 (n = 12). In group 2 (n = 33), cup volume was smaller (p = 0.020), temporal quadrant RNFL thickness was greater by 18.8 T 16.6 Km (p G 0.001), and RNFL peak angle was smaller by 18.7 T 25.3 degrees in ERM eyes compared with fellow eyes (p = 0.001). In the 15 patients in group 2 who underwent ERM removal, temporal quadrant RNFL thickness decreased and the RNFL peak angle increased after the surgery (p = 0.008 and p = 0.001, respectively). Conclusions. The configurations of the ONH and peripapillary RNFL in eyes with ERM were different from those in fellow eyes. The characteristic configurations of RNFL such as small peak angle and temporal quadrant thickening may be considered when evaluating parameters as measured by spectral domain optical coherence tomography. (Optom Vis Sci 2014;91:1328Y1334) Key Words: epiretinal membrane, optic nerve head, peripapillary retinal nerve fiber layer, spectral domain optical coherence tomography, glaucoma
M
acular epiretinal membrane (ERM) is an avascular, fibrocellular membrane that proliferates on the inner retinal surface and may lead to various degrees of visual impairment.1 Epiretinal membrane is a relatively common disease, with a prevalence of 7 to 11.8% in two large population studies.2,3 Mild forms are characterized by an abnormal retinal light reflex on fundoscopy with mild retinal thickening and no distortion of the retinal surface.4 However, in some patients, there may be progressive contraction of the ERM, resulting in distortion of the retinal surface.4,5 Although the diagnosis of an ERM is usually straightforward by fundus examination, optical coherence tomography (OCT) may be useful to diagnose ERM and to monitor the clinical course of ERMs before and after surgery.4,6Y9
*MD, PhD † MD Department of Ophthalmology, Korea University College of Medicine, Seoul, South Korea (JO); and Department of Ophthalmology, Dongguk University Ilsan Hospital, Goyang, South Korea (J-HO, JRD, MC, CYP).
In addition to the macular images, OCT can provide images of the optic nerve head (ONH) and the peripapillary retinal nerve fiber layer (RNFL). Using these images, OCT software programs automatically measure RNFL thickness at each pixel along the peripapillary circle. They also measure ONH parameters, including optic rim area, optic disc area, average cup/disc ratio, vertical cup/disc ratio, and optic cup volume.10 Chronic, progressive loss of RNFL tissue is the hallmark of glaucomatous optic neuropathy.11 The ONH is typically examined for signs of glaucomatous damage by assessing the status of the neuroretinal rim.12 Therefore, evaluation of the ONH and peripapillary RNFL using OCT is useful for the diagnosis and management of glaucoma.10,13Y15 However, previous studies reported that compounding conditions such as myopia, optic disc size, and corneal astigmatism may affect parameters of the RNFL and ONH as measured by OCT.16Y18 We hypothesized that configurations of the ONH and peripapillary RNFL could be different from those of fellow eyes. In the present study, we investigated the effect of ERM on
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al.
parameters of the ONH and the RNFL as measured by spectral domain (SD)-OCT.
METHODS This study was designed as a retrospective case series. We obtained institutional review board approval from the Dongguk University Ilsan Hospital in Goyang, South Korea. All research adhered to the tenets of the Declaration of Helsinki.
Patients and Data Collection We retrospectively reviewed the medical records of consecutive patients with macular ERM who were examined at Dongguk University Ilsan Hospital between September 2012 and August 2013. Epiretinal membrane was diagnosed by fundus examination and SD-OCT examination. Patients with high myopia (9j6 diopters), glaucoma, diabetic retinopathy, retinal vein occlusion, agerelated macular degeneration, or a history of uveitis were excluded from the study. Seventy Korean patients with idiopathic ERM were reviewed. Thirteen patients were excluded because of high myopia (three eyes), glaucoma (one eye), diabetic retinopathy (five eyes), retinal vein occlusion (one eye), age-related macular degeneration (two eyes), or a history of uveitis (one eye) in ERM eyes or fellow eyes. Twelve patients had bilateral ERM. In a total of 45 patients with unilateral ERM, ERM eyes were compared with normal fellow eyes. Epiretinal membrane removal was performed in 15 eyes from 15 patients. Of these, four eyes of four patients with bilateral ERM were included. All SD-OCT images had a signal-to-noise ratio of 0.7 or higher. Data including age, sex, best-corrected Snellen visual acuity, central subfield retinal thickness, ONH parameters, peripapillary RNFL parameters, and fundus photographic images were
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obtained. In 15 eyes that underwent ERM removal, postoperative data were also obtained. The decision to operate on the ERM was based on the patient’s macular symptoms. All surgeries were performed by a single surgeon (J-HO). A three-port 23-gauge transconjunctival sutureless vitrectomy was performed under general anesthesia using the Constellation Vision System (Alcon Laboratories, Inc, Fort Worth, TX) and the noncontact wide-angle viewing system (BIOM 3; Oculus, Wetzlar, Germany). In patients with a visually significant cataract, phacoemulsification with implantation of an intraocular lens was performed before vitrectomy. Posterior vitreous detachment was induced with active outcome suction over the optic disc if posterior vitreous detachment was not already present. Triamcinolone acetonide was used to assist visualization and removal of posterior hyaloid and ERM. After complete removal of the posterior vitreous and extensive shaving of the peripheral vitreous, the ERM was removed using end-gripping forceps. A contact lens (Hoya Corp, Tokyo, Japan) was used to view the macula. In the eight most recent cases, the internal limiting membrane (ILM) was also peeled using end-gripping forceps after indocyanine green staining.
OCT Imaging Spectral domain optical coherence tomography was performed using the Cirrus HD-OCT (Model 4000, software version 6.0, Carl Zeiss Meditec, Dublin, CA) using a wavelength of 840 nm and an axial resolution of 5 Km. All SD-OCT included a macular cube scan and an optic disc cube scan. The 512 by 128 macular cube scan produces 128 horizontal scan lines, composed of 512 A-scans per line over a 6- by 6-mm area. Central subfield retinal thickness is assessed at the macular center (1 mm diameter) using a topographic map of the macular cube scan. The 200 by 200 optic disc scan captures a 6 by 6-mm2 cube, which is formed from 200 A-scans for each of 200 B-scans. A circle 3.46 mm in diameter consisting
FIGURE 1. Measurements of the RNFL peak angle using a TSNIT curve of the Cirrus HD-OCT (left bottom). The median value of points that had the greatest RNFL thickness was determined in the superior (a) or inferior (b) side of the TSNIT curve. Then, the locations of the superior (>) and inferior (A) RNFL peak were calculated in the angular values by the following formulas: > (degrees) = a 360/256, A (degrees) = (256 j b) 360/256. The RNFL peak angle was calculated from the sum of superior and inferior peak locations. A color version of this figure is available online at www.optvissci.com. Optometry and Vision Science, Vol. 91, No. 11, November 2014
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1330 Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al.
of 256 A-scans is then automatically positioned around the optic disc. The RNFL thickness along this peripapillary circle is measured at each pixel and an RNFL thickness map is generated. Optic nerve head parameters including disc area, rim area, average cup/disc ratio, vertical cup/disc ratio, and cup volume are automatically measured.19 The disc margin is defined as the termination of the Bruch membrane. The rim width around the entire circumference of the optic disc is then determined by measuring the thickness of the neuroretinal tissue in the optic nerve as it turns to exit through the opening in the Bruch membrane. The average cup/disc ratio is calculated by taking the square root of the ratio of the cup area to the disc area. The vertical cup/disc ratio is the ratio of the cup diameter to the disc diameter in a vertical meridian through the cup center. The cup volume is a three-dimensional measurement defined as the volume between the vitreoretinal interface and a plane at a fixed offset located 200 Km from the plane of the optic disc.20 The location of superior or inferior RNFL peaks was evaluated on the RNFL temporal, superior, nasal, inferior, and temporal (TSNIT) curve of the Cirrus HD-OCT (Fig. 1).21 The median value of points with the greatest RNFL thickness was determined in the superior (a) or inferior (b) side of the TSNIT curve. The peak locations appeared as points ranging from 0 to 255, as provided by the Cirrus HD-OCT algorithm. Then, the locations of the superior (>) and inferior (A) RNFL peak were calculated in angular values by the following formulas: > (degrees) = a 360/256, A (degrees) = (256 j b) 360/256. The RNFL peak angle was calculated from the sum of superior and inferior peak locations.
statistics were two tailed, and a p value less than 0.05 was considered significant.
RESULTS OCT Parameters between Eyes with ERM and Fellow Eyes The mean (TSD) age of 45 patients with unilateral ERM was 64.1 (T8.1) years. Fifteen (33.3%) of the patients were male and 30 (66.7%) were female. Twenty-two (48.9%) of the affected eyes were right eyes and 23 (51.5%) were left eyes. Of 45 total ERM eyes, 12 (26.7%) eyes with grade 1 ERM were categorized into group 1; 28 (62.2%) eyes with grade 2 ERM and 5 (11.1%) eyes with grade 3 ERM were categorized into group 2. There were no significant differences in ONH parameters and peripapillary RNFL parameters between affected and unaffected eyes of patients in group 1 (Table 1). However, several parameters were significantly different between affected and unaffected eyes in group 2, as shown in Table 2. Epiretinal membrane eyes had smaller cup volume than fellow eyes (p = 0.020). The average RNFL thickness was 5.0 T 10.7 Km thicker in ERM eyes (p = 0.011). Although superior, inferior, and nasal quadrant RNFL TABLE 1.
Comparison of measurements between affected and unaffected eyes of patients in group 1 with ERM but no retinal distortion n = 12
ERM and OCT Parameters Epiretinal membrane severity on fundus imaging was graded based on the three-step scale used in previous studies.22Y24 Grade 1 represented visible membranes without retinal distortion, grade 2 membranes had mild-to-moderate macular striae or vessel straightening, and grade 3 membranes had moderate-to-severe striae with vascular straightening.22 Two independent observers (J-HO and JRD) graded ERM severity. If there was discordance, a third observer (CYP) decided the grade. We classified patients with grade 1 ERM within group 1 and patients with grade 2 or grade 3 ERM within group 2. Group 1 represented patients with ERM without retinal distortion, and group 2 represented patients who had ERM associated with retinal distortion. Optical coherence tomography parameters were compared between eyes with ERM and normal fellow eyes in groups 1 and 2. Several patients in group 2 underwent vitrectomy for the removal of ERM. In those cases, OCT parameters were also compared before and after the surgery.
Statistical Analyses All data were analyzed using SPSS software version 20.0 (SPSS Inc, Chicago, IL). Descriptive statistics included the mean, SD, and proportion, as appropriate. The Kolmogorov-Smirnov test was used to verify the normality of the distribution of continuous variables. For comparison between two groups, the paired t test or the Mann-Whitney U test was used for continuous variables and the Fisher exact test was used for categorical variables. All
BCVA, logMAR Snellen equivalent Central subfield retinal thickness, Km ONH parameters Rim area, mm2 Disc area, mm2 Average cup/disc ratio Vertical cup/disc ratio Cup volume, mm3 Peripapillary RNFL parameters Average thickness, Km Superior quadrant thickness, Km Inferior quadrant thickness, Km Temporal quadrant thickness, Km Nasal quadrant thickness, Km Peak angle, degrees Superior peak location, degrees Inferior peak location, degrees
ERM eyes
Fellow eyes
p
0.06 T 0.12 20/23 283.0 T 45.6
0.03 T 0.05 20/21 251.1 T 21.4
0.705
1.20 T 0.18 1.88 T 0.34 0.57 T 0.13 0.54 T 0.12 0.20 T 0.17
1.21 T 0.13 1.97 T 0.36 0.59 T 0.12 0.56 T 0.10 0.24 T 0.18
0.999 0.209 0.141 0.344 0.255
92.4 T 9.1 114.6 T 13.3
90.8 T 7.2 110.7 T 11.3
0.454 0.239
115.8 T 21.1
120.3 T 16.9
0.116
72.6 T 14.4
68.5 T 12.2
0.168
63.7 T 9.8
66.3 T 9.2
0.142
147.4 T 19.2 75.8 T 14.9
145.9 T 19.9 74.2 T 14.9
0.455 0.582
71.6 T 10.0
71.7 T 9.0
0.875
0.021
Results are expressed as mean T SD. p values were calculated with Wilcoxon signed rank test. BCVA, best-corrected visual acuity; logMAR, logarithm of the minimum angle of resolution.
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al. TABLE 2.
Comparison of measurements between affected and unaffected eyes of patients in group 2 with ERM and retinal distortion n = 33
ERM eyes
BCVA, logMAR Snellen equivalent Central subfield retinal thickness, Km ONH parameters Rim area, mm2 Disc area, mm2 Average cup/disc ratio Vertical cup/disc ratio Cup volume, mm3 Peripapillary RNFL parameters Average thickness, Km Superior quadrant thickness, Km Inferior quadrant thickness, Km Temporal quadrant thickness, Km Nasal quadrant thickness, Km Peak angle, degrees Superior peak location, degrees Inferior peak location, degrees
Fellow eyes
p
0.19 T 0.21 0.04 T 0.05 G0.001 20/31 20/22 363.4 T 101.4 244.7 T 18.6 G0.001
1.31 T 0.27 1.93 T 0.37 0.53 T 0.16 0.48 T 0.15 0.13 T 0.10
1.27 T 0.23 1.98 T 0.33 0.57 T 0.12 0.54 T 0.12 0.17 T 0.13
0.347 0.303 0.068 0.053 0.020
95.2 T 8.5 112.0 T 16.3
90.2 T 13.4 109.2 T 20.6
0.011 0.373
114.6 T 17.8
117.2 T 20.5
0.367
87.9 T 16.8
69.1 T 10.9 G0.001
66.2 T 8.9
65.4 T 13.6
130.1 T 22.9 63.6 T 15.6 66.5 T 15.7
0.710
148.8 T 20.5 G0.001 77.0 T 13.5 G0.001 71.9 T 12.9
0.066
Results are expressed as mean T SD. p values were calculated with paired t test. BCVA, best-corrected visual acuity; logMAR, logarithm of the minimum angle of resolution.
thickness did not differ between both eyes, temporal quadrant RNFL thickness was thicker in ERM eyes than in fellow eyes by 18.8 T 16.6 Km (p G 0.001). The RNFL peak angle was 18.7 T 25.3 degrees smaller in ERM eyes than in fellow eyes (p = 0.001). Although inferior RNFL peak location did not differ between affected and unaffected eyes, the superior RNFL peak location was significantly smaller in ERM eyes than in fellow eyes, a difference of 13.3 T 19.6 degrees (p G .001). Central subfield retinal thickness was significantly thicker in ERM eyes than in normal fellow eyes in both groups 1 and 2 (p = 0.021 and p G 0.001, respectively).
Before and after ERM Removal In 8 (53.3%) of 15 eyes that underwent ERM removal, ILM peeling was also performed. Twelve (80%) eyes underwent cataract surgery at the same time. Postoperative OCTs were performed 10.1 T 6.4 weeks (mean T SD) (range, 5 to 24 weeks) after the surgery. After the surgery, temporal quadrant RNFL thickness decreased and RNFL peak angle significantly increased (p = 0.008 and p = 0.001, respectively, Fig. 2). However, cup volume did not differ significantly between before and after surgery (p = 0.571). There were no significant differences in the decrease of temporal quadrant RNFL thickness or the increase of RNFL peak angle
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between groups with and without additional ILM peeling (p = 0.163 and p = 0.269, respectively).
DISCUSSION Evaluation of the ONH and peripapillary RNFL is fundamental for the diagnosis and management of glaucoma.10,13Y15 However, various factors can affect their morphology. Hwang et al.21 reported that the eyes with a myopic temporal optic disc tilt and counterclockwise rotation had a thicker temporal RNFL and a more temporally positioned superior peak location. In another study, they reported that vitreopapillary traction caused RNFL thickening.25 Other studies have reported that race, ethnicity, myopia, optic disc size, and corneal astigmatism affected parameters of the ONH and RNFL.16Y19,26Y28 In the present study, we showed that these parameters were also affected by ERM. Direct mechanical traction by a contractile ERM may affect the ONH and peripapillary RNFL beyond the macula.29 In addition, the shift of the RNFL peak toward the fovea may cause the thickened temporal quadrant RNFL.30 In the present study, the RNFL peak angle and the superior RNFL peak shifted toward to the fovea in eyes with ERM-associated retinal distortion compared with fellow eyes, although the location of the inferior RNFL peak did not differ significantly. The results of the current study suggest that the macular pathology should be evaluated in eyes with RNFL peaks shifted toward the fovea and greater temporal RNFL thickness compared with fellow eyes. Some patients have visual symptoms owing to severe ERM-related retinal distortion, and clinicians may recognize macular pathology with detailed history taking. However, other patients may have no visual symptoms even with ERM-related retinal distortion. In these cases, characteristic findings of the ONH and RNFL in eyes with ERM would be helpful in recognizing macular pathology. More advanced ERM has contractile components that exert traction on the underlying retina, distorting the retinal vasculature.4,31 In the present study, we hypothesized that contraction of the ERM may affect the ONH and peripapillary RNFL beyond the macula. Therefore, we categorized eyes with ERM into two groups based on the presence or absence of ERM-associated retinal distortion and evaluated the effect of ERM severity on parameters of the ONH and the peripapillary RNFL as measured by SDOCT. Although ONH and RNFL parameters were not affected in eyes with ERM without retinal distortion, smaller cup volume, greater temporal quadrant RNFL thickness, and smaller RNFL peak angle were observed in eyes with ERM-associated retinal distortion compared with normal fellow eyes. The results suggest that the clinicians may consider additional studies for evaluation of the ONH and RNFL in glaucomatous eyes with ERM and retinal distortion. In addition, ERM is known to be progressive. Progression from less severe ERM without retinal distortion to more severe ERM with retinal distortion was observed in 9% of patients after 5 years in an older Australian population.32 Although no parameters of the ONH and RNFL were affected in eyes with ERM without retinal distortion, those parameters may be affected if the ERM progresses to include retinal distortion. Therefore, clinicians should be aware that ERM progression may cause changes in ONH and RNFL parameters in glaucomatous eyes that have been associated with ERM without retinal distortion.
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1332 Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al.
FIGURE 2. Preoperative (right) and postoperative (left) fundus photographs and OCT images of an eye that underwent ERM removal. Six weeks after the surgery, temporal quadrant RNFL thickness decreased from 115 to 77 Km and RNFL peak angle increased from 115.3 to 136.4 degrees (bottom). A color version of this figure is available online at www.optvissci.com.
Reddy et al. investigated the change of RNFL thickness in ERM eyes that underwent vitrectomy.29 We also evaluated the effect of ERM surgery on these parameters and demonstrated that temporal quadrant RNFL thickness decreased and RNFL peak angle significantly increased after ERM removal. There is debate as to the potential benefit of completing an ILM peeling after ERM removal.4 In a previous study, ILM peeling was correlated with improved unfolding of the posterior pole in eyes operated on for ERM.33 Some surgeons may consider ILM peeling in eyes with ERM and severe retinal distortion. In the present study, however, additional ILM peeling did not affect restoration of the temporal quadrant RNFL thickness or RNFL peak angle. Further largescale studies are needed to confirm the effect of ILM peeling on
retinal topographic changes using RNFL parameters measured by SD-OCT. One major limitation of this study is the small number of cases. Inferior peak location did not differ statistically between eyes with ERM and retinal distortion and fellow eyes. The topographic location of ERM may affect this result. However, the limited number of cases prevented further analysis. Another limitation is that all patients did not routinely undergo examinations such as red-free fundus photography and a visual field test for glaucoma evaluation. However, they had a normal range of intraocular pressures and their optic discs did not appear glaucomatous. It is possible that segmentation errors in OCT software caused the thickened temporal quadrant RNFL in eyes with ERM and retinal distortion.
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Retinal Nerve Fiber Layer in Eyes with Epiretinal MembraneVOh et al.
Retinal nerve fiber layer thickness measured by SD-OCT may include the thickness of the ERM at temporal quadrant.34 Asrani et al.34 demonstrated that ocular pathologic features were the most common cause of artifacts in RNFL scans and the primary ocular pathologic feature accounting for artifacts was the presence of an ERM. Direct mechanical traction by a contractile ERM may change the configuration of the ONH, resulting in smaller cup volume. However, other ONH parameters did not differ between eyes with ERM and fellow eyes, and cup volume did not differ significantly between before and after surgery. In conclusion, the configurations of the ONH and peripapillary RNFL in eyes with high-grade ERM were different from those in fellow eyes. The characteristic configurations of RNFL such as small peak angle and temporal quadrant thickening may be considered as a confounding factor when evaluating parameters as measured by SD-OCT.
ACKNOWLEDGMENTS This research was supported by a grant from the Korean Health Technology R&D Project, Ministry of Health and Welfare, Republic of Korea (HI10C1979). Received March 2, 2014; accepted June 30, 2014.
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Jong-Hyun Oh Department of Ophthalmology Dongguk University Ilsan Hospital 27, Dongguk-ro, Ilsandong-gu Goyang, 410-773 South Korea e-mail: [email protected]
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