|Year : 2016 | Volume
| Issue : 1 | Page : 35-41
Correlation between optical coherence tomographic patterns and visual acuity in eyes with diabetic macular edema
Hossam T Al-Sharkawy
Department of Ophthalmology, Ophthalmology Center, Faculty of Medicine, Mansoura University, Mansoura, Egypt
|Date of Submission||06-May-2015|
|Date of Acceptance||13-Jun-2015|
|Date of Web Publication||16-Mar-2016|
Hossam T Al-Sharkawy
Department of Ophthalmology, Ophthalmology Center, Faculty of Medicine, Mansoura University, Mansoura 35516
Source of Support: None, Conflict of Interest: None
The aim of the present study was to investigate the correlation between different features of optical coherence tomography, macular thickness, and visual acuity (VA) in patients with diabetic macular edema.
Patients and methods
In total, 168 eyes with clinically significant diabetic macular edema were included in the study. Best-corrected VA was measured and converted to the logarithm of the minimum angle of resolution (logMAR). Optical coherence tomography was carried out and morphology at the presumed fovea was used to classify eyes into four groups: group I, in which the eyes had only noncystoid sponge-like diffuse retinal thickening (DRT); group II, in which the eyes had DRT with cystoid macular edema (CME); group III, in which the eyes had DRT with serous retinal detachment (SRD); and group IV, in which the eyes had DRT with CME and SRD in the same eye. Retinal thickness at the central fovea [center point thickness (CPT)], average macular thickness (AMT), and the height of the cystoid space and the SRD at the fovea were measured.
DRT was found alone in 65% of the eyes, CME in 16%, SRD in 13%, and CME and SRD in 6%. Mean logMAR was 0.68 with DRT, 1.16 with CME, 0.89 with SRD, and 1.05 with CME and SRD. Mean CPT was 299 μm in DRT, 573 μm in CME, 354 μm in SRD, and 483 μm in CME and SRD, whereas mean AMT was 309 μm with DRT, 374 μm with CME, 344 μm with SRD, and 390 μm with CME and SRD. There was a positive significant correlation between logMAR and CPT in DRT (0.357, P = 0.001), whereas the correlation was less in CME, SRD, and CME and SRD (0.373, P = 0.087; 0.463, P = 0.053; and 0.082, P = 0.847; respectively). The positive correlation between logMAR and AMT was significant in DRT, CME, and SRD but not in CME and SRD (0.314, P = 0.002; 0.605, P = 0.003; 0.646, P = 0.004; and 0.327, P = 0.429, respectively). The height of the SRD was positively correlated with logMAR (0.516, P = 0.028), whereas the correlation between the height of the cystoid space in CME and logMAR was less (0.360, P = 0.099).
DRT was the most common feature. CME had worst visual outcome and greatest CPT and AMT. In DRT, worse VA correlated more with CPT than with AMT, whereas in CME and SRD, correlation of VA was more with AMT than with CPT. VA correlated with height of lesion in eyes with SRD but not with CME. The height of cystoid space correlated with CPT but not with AMT, whereas the height of SRD correlated with both CPT and AMT.
Keywords: diabetic macular edema, optical coherence tomography, visual acuity
|How to cite this article:|
Al-Sharkawy HT. Correlation between optical coherence tomographic patterns and visual acuity in eyes with diabetic macular edema. Delta J Ophthalmol 2016;17:35-41
|How to cite this URL:|
Al-Sharkawy HT. Correlation between optical coherence tomographic patterns and visual acuity in eyes with diabetic macular edema. Delta J Ophthalmol [serial online] 2016 [cited 2018 Apr 23];17:35-41. Available from: http://www.djo.eg.net/text.asp?2016/17/1/35/178773
| Introduction|| |
Diabetic macular edema (DME) is the major cause of vision loss in diabetic patients . Approximately 14% of all diabetics are affected by DME, and the 10-year incidence of DME in patients with newly diagnosed type 2 diabetes is ∼20% ,. The gold standard for diagnosing DME remains the fundus slit lamp biomicroscopy . Macular edema is clinically significant, as defined by the Early Treatment Diabetic Retinopathy Study (ETDRS) protocol, if retinal thickening or hard exudate associated with adjacent retinal thickening is observed within 500 μm of the center of the foveal avascular zone or there is swelling greater than 1 disc diameter (DD) within 1 DD from the center of macula . Recently, optical coherence tomography (OCT) has been shown to be a valid method for the early detection of DME, and its use has become a new morphologic gold standard in everyday clinical practice and randomized clinical trials ,,. Using OCT it is possible to measure objectively macular thickness and investigate quantitatively the relationship between DME and visual acuity (VA) ,,. Previous studies have reported different degrees of correlation between OCT-measured retinal thickness and VA, ranging from 0.28 to 0.73 ,,,,,,,,. OCT can also provide morphologic information about DME - for example, macular thickening might be classified as cystoid macular edema (CME), serous retinal detachments (SRDs), and sponge-like retinal swelling .
The aim of this study was to investigate the correlation between the different features of OCT, macular thickness, and best-corrected VA in patients with clinically significant DME.
| Patients and methods|| |
This prospective study comprised 168 eyes of 92 patients with type 2 diabetes mellitus who had clinically significant DME and attended the outpatient clinic at the Mansoura Ophthalmic Centre, Faculty of Medicine, Mansoura University, Egypt, between March 2012 and February 2013. There were 55 (59.78%) men and 37 (40.22%) women and their ages ranged from 40 to 77 years with a mean age of 57.25 ± 8.15 years. Exclusion criteria were ocular disease apart from diabetic retinopathy such as cataract, dense nuclear sclerosis or other causes of vision loss, presence of subfoveal hard exudates, proliferative diabetic retinopathy, significant media opacities that precluded fundus examination or imaging, definite posterior hyaloid traction (PHT) or tractional retinal detachment on OCT, and prior intraocular surgery including pseudophakia, intravitreal injection, or laser photocoagulation. All patients underwent a complete ophthalmic evaluation, including anterior segment examination, posterior segment biomicroscopy with slit lamp and a fundus lens, and best-corrected VA. Macular edema was considered to be clinically significant - as defined by the ETDRS protocol  - if there was retinal thickening or hard exudates associated with adjacent retinal thickening observed within 500 ± 50 μm of the center of the foveal avascular zone or zones of retinal thickening 1 disc area or larger, any part of which was within 1 DD of the center of the macula. The visual acuities were converted to the logarithm of the minimum angle of resolution (logMAR) scale. Optical coherence tomograms were acquired through a dilated pupil by an experienced examiner. A three-dimensional, Fourier domain OCT system, which is combined with a nonmydriatic retinal camera three-dimensional OCT 1000 (Topcon Corp., Tokyo, Japan), was used in this study. This system has ∼5 μm axial resolution, 20 μm horizontal resolution, and acquires 18 700 axial scan/s corresponding to about 36 image of commercially available stratus generator (512 axial scans per image). Three-dimensional data were obtained using the raster scanning technique, centered on the fovea, covering a square area of 6 mm (horizontal), 6 mm (vertical), and 1.7 mm (axial depth). This raster pattern acquires 128 horizontal scan; each scan is composed of 512 axial scans. The total acquisition time of three-dimensional data is less than 3.7 s. A super luminescent diode with a wavelength of 840 nm and a bandwidth of 50 nm is used as a light source.
OCT enabled clear visualization of the individual layers; the presumed fovea was first defined as the central area without the inner retinal layers whether retinal detachment, cystoid spaces, or retinal swelling was present or absent. These layers, which were well delineated in the periphery, were traced to the central area until the area where these layers disappeared was determined. The retinal thickness at the central fovea, center point thickness (CPT), was defined as the distance from the inner retinal surface to the retinal pigment epithelium, even in eyes with SRD. It was automatically measured in all eyes by the computer that also measured the average macular thickness (AMT), height of the cystoid space, and height of the SRD in eyes with CME and/or SRD, as shown in Figs 2-4. The classification proposed by Otani et al.  and Murakami et al.  of the morphology at the presumed fovea was used to classify the pathology into four groups:
- Group I, in which the eyes had noncystoid sponge-like diffuse retinal thickening (DRT), which showed increased retinal thickness with reduced intraretinal reflectivity and expanded areas of lower reflectivity in the outer retinal layers without CME or SRD [Figure 1].
- Group II, in which the eyes had DRT with CME defined by the presence of intraretinal cystoid-like spaces that appeared as round or oval areas of low reflectivity, with highly reflective septa separating the cystoid-like cavities [Figure 2].
|Figure 2: Cystoid macular edema at the presumed fovea; 519 μm represents the height of the cystoid space at the presumed fovea.|
Click here to view
- Group III, in which the eyes had DRT with SRD represented as thickening of the fovea with subfoveal fluid accumulation and a distinct outer border of the detached retina without foveal traction [Figure 3].
|Figure 3: Serous retinal detachment at the presumed fovea; 295 μm represents the height of serous retinal detachment at the presumed fovea.|
Click here to view
- Group IV, in which the eyes had DRT with CME and SRD in the same eye [Figure 4].
|Figure 4: Cystoid macular edema and serous retinal detachment at the presumed fovea; 311 ޤm represents the height of the cystoid space and 247 μm represents the height of the serous retinal detachment at the presumed fovea.|
Click here to view
Observed data were presented as mean and SD, and statistical analysis was carried out using a statistical software package (SPSS 15.0 for Windows; SPSS Inc., Chicago, Illinois, USA). Multiple values were compared by the analysis of variance; when differences were significant, post-hoc multiple comparisons were carried out (LSD test), whereas correlations were investigated using Spearman's correlation coefficient. A P value of less than or equal to 0.05 was considered statistically significant.
| Results|| |
The best-corrected VA in all eyes expressed in logMAR ranged from 0.00 to 2.40 with a mean of 0.80 ± 0.43. The mean CPT was 360.28 ± 174.16 μm with a range from 153 to 891 μm, whereas the mean AMT was 328.83 ± 67.41 μm with a range from 212.70 to 512.70 μm. There was a significant positive correlation between logMAR and CPT (0.530, P = 0.000) and AMT (0.526, P = 0.000).
OCT scans at the presumed fovea of the 168 eyes included in the study showed DRT alone in 109 eyes (64.88%, group I), with CME in 27 eyes (16.07%, group II), with SRD in 22 eyes (13.10%, group III), and with CME and SRD in the same eye in 10 eyes (5.95%, group IV).
[Table 1] shows the number and percentage of eyes and age of patients in the four groups. There was no statistically significant difference in the age between the four groups (P = 0.845).
[Table 2] shows the VA expressed in logMAR for the four groups. There was a significant difference in VA between groups (P = 0.000). The mean VA was best in group I (DRT only: 0.68 ± 0.42) and worst in group II (CME: 1.16 ± 0.28).
|Table 2: Visual acuity (logarithm of the minimum angle of resolution) in the four groups|
Click here to view
[Table 3] shows the CPT in the four groups. There was a significant difference in CPT between groups (P = 0.000). The mean CPT was least in group I (DRT only: 299.35 ± 137.20 μm) and most in group II (CME: 573.14 ± 155.34 μm). There was a significant positive correlation between logMAR and CPT for the eyes in group I (with DRT only) (P = 0.001, i.e. increased CPT correlated with worse VA) but the correlation in the other three groups was not statistically significant.
|Table 3: Center point thickness in the four groups and its correlation with logarithm of the minimum angle of resolution|
Click here to view
[Table 4] shows the AMT in the four groups. There was a significant difference in AMT between groups (P = 0.000). The mean AMT was least in group I (DRT only: 309.44 ± 59.87 μm) and most in group IV (CME and SRD: 389.73 ± 59.31 μm). The positive correlation between logMAR and AMT was statistically significant in groups I, II, and III (P = 0.002, 0.003, and 0.004, respectively - i.e. increased AMT correlated with worse VA) but not in the eyes in group IV.
|Table 4: Average macular thickness in the four groups and its correlation with logarithm of the minimum angle of resolution|
Click here to view
[Table 5] shows the height of the cystoid space at the presumed fovea in eyes with CME only (group II) or associated with SRD (group IV), and also the height of SRD at the presumed fovea in eyes with this lesion only (group III) or associated with CME (group IV). The correlation between the height of the cystoid space and logMAR was not significant in neither group II nor group IV (P = 0.099 and 0.096, respectively), whereas there was a significant positive correlation between the height of the SRD and logMAR in eyes of patients in group III but not group IV (P = 0.028 and 0.470, respectively).
|Table 5: Height of cystoid space and serous retinal detachment at the presumed fovea and their correlation with logarithm of the minimum angle of resolution, center point thickness and average macular thickness|
Click here to view
There was a positive significant correlation between the height of the cystoid space and CPT in eyes of group II but not group IV (P = 0.001 and 0.651, respectively); furthermore, the positive correlation between the height of the SRD and CPT was significant in eyes of group III but not group IV (P = 0.000 and 0.779, respectively).
The correlation between the height of the cystoid space and AMT was not significant, neither in group II nor in group IV (P = 0.089 and 0.493, respectively), whereas there was a significant positive correlation between the height of the SRD and AMT in eyes of group III but not group IV (P = 0.000 and 0.352, respectively).
| Discussion|| |
OCT is a noninvasive, quick, and reproducible method of producing high-resolution, cross-sectional images of the retina ,,,,,. It has specifically been utilized for the morphologic analysis of DME ,, and has disclosed that DME includes three basic structural changes, namely retinal swelling, CME, and SRD .
In the current study, DRT occurred alone in 64.88% of the eyes, whereas CME was found in 16.07% of the eyes, SRD in 13.10%, and CME and SRD in the same eye in 5.95%. DRT was also the most common feature in previous reports that studied the OCT patterns of DME. In their study, Otani et al.  found DRT in 88% of the eyes, CME in 47%, and SRD in 15%, whereas Yamamoto et al.  in their study reported DRT in 60% and CME in 40% of the eyes with DME. A study by Murakami et al.  also classified three types of pathomorphology at the presumed fovea: CME (CME type: 16%), SRD (SRD type: 16.8%), and the absence of either CME or SRD (diffuse type: 67.2%).
However, Kim et al. , in another study, described five morphologic patterns of DME: DRT (97%), CME (55%), SRD without PHT (7.0%), PHT without traction retinal detachment (12.7%), and PHT with traction retinal detachment (2.9%).
It has long been established that central macular thickening can be associated with a decrease in VA . In the present study, there was a significant negative correlation between VA with best correction and each of CPT and AMT. The CPT was significantly greater in eyes with CME than in those with DRT alone or with SRD, whereas AMT was significantly greater in eyes with CME than in those with DRT alone; best-corrected VA was significantly worse in eyes with CME than in those with DRT alone. The current study revealed a strong negative correlation between best-corrected VA and CPT at the presumed fovea in eyes with diffuse thickening alone, whereas the correlation was not significant in eyes associated with CME or SRD or both. Conversely, the negative correlation between best-corrected VA and AMT was strong in eyes with diffuse thickening alone and in those associated with CME or SRD.
These results were comparable to previous studies, which showed modest correlation between OCT-measured CPT and VA . In their study, Yamamoto et al.  found that the fovea of the eyes with cystoid edema was significantly thicker than the fovea of eyes with diffuse swelling. In the study by Kim et al. , the mean retinal thickness and mean visual acuities also varied between groups, depending on the morphologic pattern; increasing retinal thickness in all patterns was significantly correlated with worse VA, and Otani et al. , in their study, also reported that the retinal thickness at the central fovea and the VA with best correction showed an intermediate negative correlation regardless of the different tomographic features, whereas Murakami et al.  concluded that the mean logMAR VA with the CME type was significantly worse than with the SRD type or diffuse type but found that parafoveal thickening was significantly correlated with poor VA in CME type and diffuse type but not in the SRD type.
More recent studies have evaluated the relationship between visual function and microstructural changes in the fovea inner segment-outer segment (IS/OS) junction and external limiting membrane (ELM) in DME. In their study, Uji et al.  found that the presence of hyper-reflective foci in the outer retina was closely associated with a disrupted ELM and IS/OS junction line on SD-OCT images and decreased VA in DME. Shin et al.  suggested that IS/OS junction and ELM were useful hallmarks in the evaluation of foveal photoreceptor layer integrity, and were closely associated with final VA in DME. Chhablani et al.  reported that the evaluation of ELM before pars plana vitrectomy predicted the vision improvement more accurately than did the IS/OS junction and CPT in eyes with DME, whereas Shen et al.  concluded that both IS/OS junction and ELM integrity correlated positively with visual function in DME patients.
The retina is a compact tissue composed of a neural element and glial cells . Because glial cells occupy all the interneural space, extracellular space is virtually absent. Histopathologic studies by Yanoff et al.  suggest that the development of macular edema is initiated because of fluid accumulation within Muller's cells. Sponge-like swellings in the OCT image may represent intracytoplasmic swelling of Muller's cells. If retinal edema persists, liquefaction necrosis of the Muller's cells ensues. Necrosis of the Muller's cells and adjacent neural cells leads to cystoid cavity formation in the retina . In the histopathologic study of CME, Tso  demonstrated that cystoid spaces were located not only in the outer plexiform layer but also in the inner plexiform and granular layers and even in the ganglion cell layer. As suggested by Yamamoto et al. , these histopathologic findings explain why those eyes with CME may be associated with worse visual outcomes compared with other subgroups of DME. Recently, Sun et al.  have also found that disorganization of the retinal inner layers in the 1-mm foveal area is associated with worse VA.
The current study also investigated the height of the cystoid space in eyes with CME and the height of the detachment in eyes with SRD at the presumed fovea and its correlation with VA, CPT, and AMT. It was found that in eyes with CME, the height of the cystoid space was not significantly correlated with VA or AMT but the correlation with CPT was significantly positive, whereas in eyes with SRD, there was a significant negative correlation between the height of the detachment and VA and a significant positive correlation between the height of the detachment and each of CMT and AMT. In eyes with combined CME and SRD, these correlations were not found. The pathological changes occurring in CME might have contributed to worse VA regardless of the height of the cystoid space, and this may explain why there was no significant correlation between the cystoid space height and VA, while there was a significant correlation between the SRD height and VA. Murakami and Yoshimura  reported the clinical relevance of the central retinal thickness in DME and suggested the presence of other factors that affected visual disturbance. They said that photoreceptor damage at the fovea was thought to be represented by disruption of the ELM or the junction between the IS and OS of the photoreceptors, and was correlated with visual impairment.
In summary, OCT disclosed three basic changes of DME, including sponge-like retinal swelling, CME, and SRD. DRT was the most common feature and CME had the worst visual outcome and greatest CPT and AMT. Generally, the VA negatively correlated with CPT and AMT. In DRT, VA correlated more with CPT than with AMT, whereas in CME and SRD, the correlation of VA was more with AMT than with CPT. The VA correlated with the height of the lesion in eyes with SRD but not with CME. The height of the cystoid space correlated with CPT but not with AMT, whereas the height of SRD correlated with both CPT and AMT.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Vujosevic S, Casciano M, Pilotto E, Boccassini B, Varano M, Midena E. Diabetic macular edema: fundus autofluorescence and functional correlations. Invest Ophthalmol Vis Sci 2011; 52:442-448.
Girach A, Lund-Andersen H. Diabetic macular oedema: a clinical overview. Int J Clin Pract 2007; 61:88-
Voutilainen-Kaunisto R, Teräsvirta M, Uusitupa M, Niskanen L. Maculopathy and visual acuity in newly diagnosed type 2 diabetic patients and non-diabetic subjects: a 10-year follow-up study.
Acta Ophthalmol Scand 2001; 79:163-168.
Hee MR, Puliafito CA, Duker JS, Reichel E, Coker JG, Wilkins JR, et al
. Topography of diabetic macular edema with optical coherence tomography. Ophthalmology 1998; 105:360-370.
Strøm C, Sander B, Larsen N, Larsen M, Lund-Andersen H. Diabetic macular edema assessed with optical coherence tomography and stereo fundus photography. Invest Ophthalmol Vis Sci 2002; 43:241-
Browning DJ, McOwen MD, Bowen RM Jr, O'Marah TL. Comparison of the clinical diagnosis of diabetic macular edema with diagnosis by optical coherence tomography.
Ophthalmology 2004; 111:712-715.
Virgili G, Menchini F, Dimastrogiovanni AF, Rapizzi E, Menchini U, Bandello F, Chiodini RG Optical coherence tomography versus stereoscopic fundus photography or biomicroscopy for diagnosing diabetic macular edema: a systematic review. Invest Ophthalmol Vis Sci 2007; 48:4963-
Hee MR, Puliafito CA, Wong C, Duker JS, Reichel E, Rutledge B, et al
. Quantitative assessment of macular edema with optical coherence tomography. Arch Ophthalmol 1995; 113:1019-1029.
Goebel W, Kretzchmar-Gross T. Retinal thickness in diabetic retinopathy: a study using optical coherence tomography (OCT). Retina 2002; 22:759-767.
Bandello F, Polito A, Del Borrello M, Zemella N, Isola M 'Light' versus 'classic' laser treatment for clinically significant diabetic macular oedema. Br J Ophthalmol 2005; 89:864-870.
Otani T, Kishi S. Tomographic findings of foveal hard exudates in diabetic macular edema. Am J Ophthalmol 2001; 131:50-54.
Martidis A, Duker JS, Greenberg PB, Rogers AH, Puliafito CA, Reichel E, Baumal C Intravitreal triamcinolone for refractory diabetic macular edema. Ophthalmology 2002; 109:920-927.
Laursen ML, Moeller F, Sander B, Sjoelie AK. Subthreshold micropulse diode laser treatment in diabetic macular oedema. Br J Ophthalmol 2004; 88:1173-1179.
Catier A, Tadayoni R, Paques M, Erginay A, Haouchine B, Gaudric A, Massin P. Characterization of macular edema from various etiologies by optical coherence tomography. Am J Ophthalmol 2005; 140:200-206.
Ozdemir H, Karacorlu M, Karacorlu SA. Regression of serous macular detachment after intravitreal triamcinolone acetonide in patients with diabetic macular edema. Am J Ophthalmol 2005; 140:251-255.
Massin P, Duguid G, Erginay A, Haouchine B, Gaudric A. Optical coherence tomography for evaluating diabetic macular edema before and after vitrectomy. Am J Ophthalmol 2003; 135:169-177.
Otani T, Kishi S, Maruyama Y. Patterns of diabetic macular edema with optical coherence tomography. Am J Ophthalmol 1999; 127:688-693.
[No authors listed]. Early Treatment Diabetic Retinopathy Study design and baseline patient characteristics. ETDRS report number 7. Ophthalmology 1991; 98(Suppl): 741-756.
Murakami T, Nishijima K, Sakamoto A, Ota M, Horii T, Yoshimura N. Association of pathomorphology, photoreceptor status, and retinal thickness with visual acuity in diabetic retinopathy. Am J Ophthalmol 2011; 151:310-317.
Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W, et al
. Optical coherence tomography. Science 1991; 254(5035): 1178-1181.
Puliafito CA, Hee MR, Lin CP, Reichel E, Schuman JS, Duker JS, et al
. Imaging of macular diseases with optical coherence tomography. Ophthalmology 1995; 102:217-229.
Hee MR, Puliafito CA, Wong C, Reichel E, Duker JS, Schuman JS, et al
. Optical coherence tomography of central serous chorioretinopathy. Am J Ophthalmol 1995; 120:65-74.
Hee MR, Puliafito CA, Wong C, Duker JS, Reichel E, Schuman JS, et al
. Optical coherence tomography of macular holes. Ophthalmology 1995; 102:748-756.
Yamamoto S, Yamamoto T, Hayashi M, Takeuchi S. Morphological and functional analyses of diabetic macular edema by optical coherence tomography and multifocal electroretinograms. Graefes Arch Clin Exp Ophthalmol 2001; 239:96-101.
Kang SW, Park CY, Ham DI. The correlation between fluorescein angiographic and optical coherence tomographic features in clinically significant diabetic macular edema. Am J Ophthalmol 2004; 137:313-322.
Kim BY, Smith SD, Kaiser PK. Optical coherence tomographic patterns of diabetic macular edema. Am J Ophthalmol 2006; 142:405-412.
Browning DJ, Glassman AR, Aiello LP, Beck RW, Brown DM, Fong DS, et al
. Diabetic Retinopathy Clinical Research Network Relationship between optical coherence tomography-measured central retinal thickness and visual acuity in diabetic macular edema. Ophthalmology 2007; 114:525-536.
Uji A, Murakami T, Nishijima K, Akagi T, Horii T, Arakawa N, et al
. Association between hyperreflective foci in the outer retina, status of photoreceptor layer, and visual acuity in diabetic macular edema. Am J Ophthalmol 2012; 153:710-717.717.e1
Shin HJ, Lee SH, Chung H, Kim HC. Association between photoreceptor integrity and visual outcome in diabetic macular edema. Graefes Arch Clin Exp Ophthalmol 2012; 250:61-70.
Chhablani JK, Kim JS, Cheng L, Kozak I, Freeman W. External limiting membrane as a predictor of visual improvement in diabetic macular edema after pars plana vitrectomy. Graefes Arch Clin Exp Ophthalmol 2012; 250:1415-1420.
Shen Y, Liu K, Xu X. Correlation between visual function and photoreceptor integrity in diabetic macular edema: spectral-domain optical coherence tomography. Curr Eye Res 2015; 21:1-9.
Hogan MJ, Alvarado JA, Weddell JE. Histology of the human eye
. Philadelphia: WB Saunders; 1971; 492.
Yanoff M, Fine BS, Brucker AJ, Eagle RC Jr. Pathology of human cystoid macular edema. Surv Ophthalmol 1984; 28(Suppl):505-511.
Fine BS, Brucker AJ. Macular edema and cystoid macular edema. Am J Ophthalmol 1981; 92:466-481.
Tso MOM. Pathology of cystoid macular edema. Ophthalmology 1982; 89:902-915.
Sun JK, Lin MM, Lammer J, Prager S, Sarangi R, Silva PS, Aiello LP. Disorganization of the retinal inner layers as a predictor of visual acuity in eyes with center-involved diabetic macular edema. JAMA Ophthalmol 2014; 132:1309-1316.
Murakami T, Yoshimura N. Structural changes in individual retinal layers in diabetic macular edema. J Diabetes Res 2013; 2013:920713.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]