Long-term capillary changes in areas of dissociated optic nerve fibre layer after macular hole surgery.

Abstract

Internal limiting membrane (ILM) peeling for macular hole (MH) surgery may cause retinal abnormalities, visible on blue-filter fundus photographs as arcuate, slightly dark, extramacular striae along the course of retinal nerve fibres. This feature, showing a dissociated optic nerve fibre layer (DONFL) appearance, perfectly corresponds to focal dehiscences (‘dimplings’) in the retinal nerve fibre layer (RNFL) on B-scan optical coherence tomography (OCT) and to concentric macular dark spots on en-face scan OCT. Although such retinal changes seem not to preclude a good visual outcome, their origin is still unclear (Tadayoni et al. 2001). We report herein the long-term capillary changes occurring in DONFL areas in 38 MH patients (16 men, 22 women) treated with ILM peeling technique. All subjects underwent extensive ophthalmic examination and retinal imaging, including structural OCT, OCT angiography and colour-coded perfusion maps, before and after surgery. En-face OCT angiograms of the superficial capillary plexus (SCP) were evaluated and compared with structural OCT findings. All angiograms and OCT images were exported into a validated custom measurement software (ImageJ software version 1.50, National Institutes of Health, Bethesda, MD). En-face scan OCT of SCP slabs was binarized by Otsu’s method. DONFL location was automatically delineated, and DONFL edges were semi-automatically overlapped on the corresponding colour-coded perfusion maps. Finally, vascular perfusion density (VPD) values of each retinal sector were correlated with the corresponding DONFL area. All eyes were followed-up postoperatively for a mean of 25.2 ± 3.2 months (range 24–29 months). Anatomical MH closure was achieved in 37/38 (97.4%) eyes. At the last follow-up examination, 34/38 (89.5%) eyes had DONFL areas, mainly in the temporal macula. Overlapping of delineated DONFL areas with colour-coded perfusion maps showed a perfect correspondence between temporal DONFL areas and no-flow regions in the temporal SCP, whereas no such correspondence was found in other SCP sectors (Table 1). Macular changes following ILM peeling are still poorly understood. Muller cell (MC) footplates are in direct contact with RNFL bundles and contribute to ILM formation. The mechanical trauma secondary to ILM peeling is likely to cause an injury to these structures, resulting in axon swelling and gaps in the RNFL, which appear as DONFL areas. Furthermore, petechial haemorrhages, often occurring on the retinal surface during ILM peeling, could be the result of direct injury to SCP vessels. DONFL areas usually appear 1–3 months after surgery in the temporal macula, where MC footplates are more numerous, progressively increase in the following 3–6 months and completely surround the fovea within 12 months (Alkabes et al. 2011; Navajas et al. 2020). Thereafter, progressive regeneration of MC footplates and DONFL attenuation may occur (Nakamura et al. 2003; Kishimoto et al. 2011). In our study, DONFL areas were still detectable in the temporal sectors after two years, thus suggesting that macular restoration may have started nasally. Furthermore, we found a statistically significant correlation between the total area of DONFL and VPD values only in the temporal SCP. Overall, these findings support the idea that retinal reparation begins with SCP regeneration and is later followed by MC footplates restoration, with final attenuation and disappearance of DONFL. Accordingly, we hypothesize three steps in the process of retinal reparation after MH surgery: (1) development of roundish no-flow regions on colour-coded perfusion maps and DONFL areas on en-face scan OCT in the temporal SCP, where both vessels and MC have been damaged; (2) persistence of DONFL areas corresponding to normal perfusion regions (superior-middle, superior-nasal, inferior-middle and inferior-nasal sectors of the SCP), because vessel restoration has been completed, but MC is still damaged; and (3) injury to SCP vessels and MC has been completely restored and neither DONFL areas nor no-flow regions can be found (intermediate-nasal sector). Further larger prospective studies are warranted to confirm this theory and fully understand the pathogenesis underlying macular changes secondary to ILM peeling in MH patients.