Structural analysis of retinal photoreceptor ellipsoid zone and postreceptor retinal layer associated with visual acuity in patients with retinitis pigmentosa by ganglion cell analysis combined with OCT imaging

Abstract

The aim of this study was to examine changes in photoreceptor ellipsoid zone (EZ) and postreceptor retinal layer in retinitis pigmentosa (RP) patients by ganglion cell analysis (GCA) combined with optical coherence tomography (OCT) imaging to evaluate the structure-function relationships between retinal layer changes and best corrected visual acuity (BCVA). Sixty-eight eyes of 35 patients with RP and 65 eyes of 35 normal controls were analyzed in the study. The average length of EZ was 911.1 ± 208.8 μm in RP patients, which was shortened with the progression of the disease on the OCT images. The average ganglion cell-inner plexiform layer thickness (GCIPLT) was 54.7 ± 18.9 μm in RP patients, while in normal controls it was 85.6 ± 6.8 μm. The GCIPLT in all quarters became significantly thinner along with outer retinal thinning. There was a significantly positive correlation between BCVA and EZ (r = -0.7622, P < 0.001) and GCIPLT (r = -0.452, P < 0.001). Therefore, we assess the retinal layer changes from a new perspective in RP patients, which suggests that EZ and GCIPLT obtained by GCA combined with OCT imaging are the direct and valid indicators to diagnosis and predict the pathological process of RP.

Figure 1

Characteristics of retinitis pigmentosa. (A) Fundus photograph with a black line (arrow) indicates the direction of the horizontal scan. (B) A shortened ellipsoid zone (white arrow) can be seen; the best corrected visual acuity was 0.5. (C) The extent of the visual field was less than 15°. (D) Electroretinography responses were almost nonrecordable.

Figure 2

Thickness map and macular retinal ganglion cell–inner plexiform layer (GCIPL) thickness. The ganglion cell analysis algorithm identifies the outer boundaries of retinal nerve fiber layer and inner plexiform layer, between which is the GCIPL layer. (A) Representative case of normal subject (left eye of 50-year-old male). (B) Representative case of retinitis pigmentosa (RP) patient (left eye of 54-year-old male). The images showed that RP patients had thinner GCIPL thickness compared with normal controls in 6 sectors.

Figure 3

Ganglion cell–inner plexiform layer thickness (GCIPLT) and outer retinal thickness (ORT) measurements. (A) Representative optical coherence tomography image of a right eye in 6 sectors (superonasal, superior, superotemporal, inferotemporal, inferior, and inferonasal). (B) GCIPL thickness was measured using the Cirrus linear measurement tool at 6 locations. Compared with healthy eyes, the thickness of the ganglion cell–plexiform layer in various quadrants was significantly thinner in retinitis pigmentosa patients. ORT was defined as a region from the outer plexiform layer to the retinal pigment epithelium layer/Bruch complex. The thickness of the outer retina was classified into 3 grades according to the statistical percentile (33.3% and 66.6%) of GCIPLT. (C) The results showed that the thinning of GCIPLT was coincident with the thinning of ORT (P < 0.001). (D) The correlation between GCIPLT and ORT was significant when evaluated by a linear regression model (r = 0.436, P < 0.001).

Figure 4

Peripapillary retinal nerve fiber layer (RNFL) thickness measurements. (A) Representative papillary optical coherence tomography image of a right eye in retinitis pigmentosa (RP) patient with RNFL thickness map and RNFL thickness values in different regions. (B)The results showed that peripapillary RNFL thicknesses did not differ significantly between the RP and control groups, but in the temporal and nasal quadrants, the RP group had a significantly thicker RNFL, while RNFL thinning was seen in the superior and inferior areas. However, total RNFL thickness was greater in the superior and inferior areas than in the temporal and nasal areas.

Figure 5

Ellipsoid zone (EZ) and extend limiting membrane (ELM) line. Grayscale images were used for the measurement of the EZ and ELM. Length was measured in the horizontal and vertical scans, and an average value was obtained. (A) The disrupted photoreceptor EZ (^∗) and ELM (^#) can be seen in the optical coherence tomography imagine. (B) Mean lengths of the EZ and ELM lines in 68 eyes with retinitis pigmentosa. ELM length was significantly greater than EZ length (P < 0.005, t = −3.107). (C) There is a significant positive correlation between the lengths of the EZ and ELM lines (r = 0.862, P < 0.001).

Figure 6

Relationship between best corrected visual acuity (BCVA) and central fovea thicknesses (CFT), ganglion cell–inner plexiform layer thickness (GCIPLT), and ellipsoid zone (EZ). CFT and GCIPLT were graded from 1 to 3 according to statistical percentile (33.3% and 66.6%). The appearance of the EZ in the optical coherence tomography (OCT) images was graded from 1 to 3: Grade 1, shortened EZ greater than 1 mm; Grade 2, shortened EZ less than 1 mm; and Grade 3, EZ not visible. Mean visual acuity (log MAR units) as a function of the grade of the OCT parameters. (A1–C1) The difference among the 3 groups was statistically significant (P < 0.005). Retinitis pigmentosa patients with thicker CFT and GCIPLT and longer EZ had better BCVA (P < 0.001). (A2–C2) The correlations among BCVA and CFT, GCIPLT, and EZ were evaluated using a linear regression model. The results showed significant positive correlations among BCVA and CFT (r = −0.5933, P < 0.001), GCIPLT (r = −0.452, P < 0.001), and EZ (r = −0.7622, P < 0.001); EZ at the fovea demonstrated a stronger relationship with BCVA.