ERM-induced tractional force can involve a broad spectrum of macular complications, ranging from thickened retinal layers, macular schisis to the formation of lamellar holes, or full-thickness macular holes. In our study, we identified an abnormal centripetal displacement of inner foveal layers by ERM traction. There is significant thickening in the inner retinal layers and a dramatic thickness reduction of the inner retinal layers after surgery. These results revealed that persistent mechanical traction in ERM affected both the inner retinal thickness and morphological retinal structure . Furthermore, a greater thickness of the GCL + IPL played an important role in predicting worse postoperative BCVA performance.
The exact mechanism by which the epiretinal membrane exerts traction at the vitreoretinal surface remains unknown. There is pathological evidence that despite evidence of a Weiss ring, remnants of the vitreous cortex can still be found on the retinal surface, indicating the presence of vitreoschisis. Gandofer et al. further proposed two different separation planes can cause different types of ERM traction ; One type of traction is that in the presence of vitreoschisis, ERM was proliferated on top of the residual vitreous cortex, and ILM was left uninvolved underneath the vitreous cortex during membrane peeling. This type of traction demonstrated with loose vitreoretinal attachment and gaps between the ILM and ERM might be identified on SD-OCT. The other traction occurs when the ERM directly adheres to the ILM. The second type of adhesion should exert stronger traction on the retina and increase the macular structure. Therefore, based on the pathological observations, we applied topographic features of the vitreoretinal surface to classify the traction pattern and correlate it with disease severity.
Tangential traction of ERM may lead to retinal surface folding, thickening of inner retinal layers and centripetal displacement of inner retina. The traction of ERM directly forced movement of the underlying inner retinal layers towards the foveal center resulting in disappearance of fovea pit and elevation of inner retinal layer of foveal walls . The importance of traction from ERM for thickening of the inner retinal layers is manifested by the data shown in Fig. 2 in which only GCL + IPL and INL were thickened but not ORL. As for the inner retinal layer, the more proximal layers near ERM, was the primary affected site of ERM-associated mechanical force. The strength of mechanical stress is in proportion to thickening of retinal layers. Our study demonstrated significantly thicker GCL + IPL thickness and INL thickness in patients with type 2 ERM than in type 1 patients. This is compatible with our hypothesis that the tight adherent epiretinal membrane exerts more anteroposterior and tangential force directly to the proximal inner retina. This imbalance in thickness contributes to the cause of visual impairment.
There is controversary regarding prognostic factors of visual outcome after ERM surgery. The integrity of photoreceptors and ellipsoid zone disruption were identified to be correlated with visual acuity . More recent studies revealed the role of inner retinal layers in vision loss. GCL + IPL layer thickening was significantly related to poor visual acuity in many reports [10, 12]. Our study showed that postoperative visual acuity was inversely correlated with the thickness of the GCL + IPL layer (Table 4).
The decreased acuity of ERM eyes was also associated with the ectopic inner foveal layers and disappearance of fovea pit which changes the light transmission and spatial resolution through the fovea . During development, centrifugal migration of inner retinal neurons is necessary to differentiate the fovea from the surrounding retina and reduce the light scattering to ensure sharp visual acuity . The ERM-mediated displacement of inner retinal layers is a pathologically inverse process compared to developmental eyes and mal-adapted contour revision under ERM traction. Our results showed ERM-induced centripetal displacement of inner retinal layers including GCL + IPL and INL across the central fovea and this ectopic inner retinal layer does not restore even after ERM peeling. Our study also suggested clinical implication that the presence of thicker ectopic inner foveal layer was accompanied with worse vision acuity and limited postoperative visual recovery. In addition, the higher index of suspicion for surgical-induced retinal injury should exist that tight adhesion ERM bridging retinal surface exerts stronger force over underlying retina. Together with these results, the visual acuity was dependent on both thickness of the inner retina and the integrity of photoreceptors.
The inner retinal thickness decreased after vitrectomy with ERM peeling, as in our case, the presence of ectopic inner retinal layer persisted with the decreased foveal thickness over postoperative period. There were still unknown causes for the failure of complete recovery of normal fovea shape after ERM peeling. One reason was upregulation of glial intermediate filaments and GFAP of muller cells increases the stiffness of the tissue and impairs the competence of movement . Another possible explanation was muller cells were pulled by the ERM traction centripetally and this impaired the centrifugal tissue movement for normal foveal contour.
There are several limitations of our study. Firstly, this study was small sample size, especially after excluding cataract interference. Secondly, ERM generates uneven traction over different meridians, but our OCT images were measured only along scan’s x axis. The lack of information on retinal thickness at different meridians could be a limitation of our study. Finally, severe ERM traction causes foveaschisis and significant retinal layer disorganization. Segmentation failure for each retinal layer often occurred and we did exclude cases from artifact analysis. This could lead to selection bias and loss some pathological steps in the developmental ERM. Therefore, our findings that preoperative thicker GCL + IPL layers in type 2 ERM was a prognostic factor for the degree of VA damage are only applicable to patients with relatively intact retinal layers.
The inner retina, particularly the GCL + IPL layer, has a larger thickness in idiopathic ERM and can be regarded as a prognostic factor for postoperative visual acuity. The fovea-occupying ectopic inner retinal layer was also worth noting in the OCT-based thickness profile. These results suggest the importance of inner retinal layers in the visual outcome of ERM.
Our study is one of the first to apply the morphological classification of SD-OCT images to ERM patients and found that type 2 tight adherent ERM patients truly exhibit thicker GCL + IPL thickness than type 1 loosely attached ERM patients. Obtaining the GCL + IPL thickness data can be time-consuming and thickening or abnormal displacement of the layer can be ambiguous to the parafovea normal retinal structure in real-world clinical settings. The clinical significance of this study is to help clinicians to speculate which group of patients may yield better anatomical and visual outcomes at the first glance of the OCT image.