Methods

In this observational study, we included all consecutive patients with a diagnosis of LMH examined at the Department of Ophthalmology, University of Catania, Catania, Italy, and at the Fondazione G.B. Bietti, IRCCS, Rome, Italy, between January 2010 and May 2011. LMH were diagnosed based on SD OCT characteristics proposed by Witkin and associates. Patients were enrolled if the following characteristics were present in at least 1 of the scans: (1) an irregular foveal contour; (2) a break in the inner fovea; (3) separation of the inner from the outer foveal retinal layers, leading to an intraretinal split; (4) absence of a full-thickness foveal defect.

Exclusion criteria were the presence in the affected eye of refractive errors of more than ± 5 diopters, astigmatism of more than 2 diopters, history of amblyopia, age-related macular degeneration, diabetes mellitus, retinal vascular occlusion, vitreous hemorrhage, a history of intraocular surgery other than uncomplicated cataract surgery, significant cataract graded at more than N03 or NC3 according to the Lens Opacity Classification Scheme, and eyes with low-quality, unreliable OCT images. In cases of bilateral LMH, 1 eye was selected randomly.

All subjects received a complete ophthalmologic examination, including the measurement of BCVA, slit-lamp biomicroscopy, intraocular pressure determination, binocular indirect ophthalmoscopy, and fundus photography. BCVA was measured using Early Treatment Diabetic Retinopathy Study charts at 4 m distance by a single, independent, well-trained, experienced orthoptist in each center who was masked to the study. Vision results were quantified in logarithm of the minimal angle of resolution units. Each patient, on the same day, first underwent microperimetry and then underwent SD OCT examination.

In both centers, the MP-1 microperimeter (Nidek Technologies, Padua, Italy) was used. After the pupils were dilated (1% tropicamide), a reference frame was obtained with the integrated infrared camera. We used a 4-2 double-staircase test strategy with white background illumination set at 4 apostilbs and the starting stimulus light attenuation set at 10 dB. Then, a grid of 45 stimuli with a Goldmann III stimulus size and a time between stimuli of 1 second was projected onto the central 8 degrees. A bright red cross of 2 degrees was used for the fixation target. For assessment of fixation, the fundus movements were tracked during examination. The patient’s mean retinal sensitivity (total sensitivity) and the mean sensitivity of the central 13 points within 2 degrees (central sensitivity) was calculated. Fixation stability was calculated as the percentage of fixation points within the 2-degree diameter circle. In all patients, microperimetry was performed twice within 1 week to rule out potential learning effects, and the second test was used for the analysis. Patients underwent a brief training session at the beginning of each test. All imaging sessions were performed after 5 minutes of visual adaptation. At each center, the examinations were carried out by the same experienced ophthalmologists (M.T., Catania; A.C., Rome). Both participating centers used the same MP1 software version (version 1.4.2). To avoid bias resulting from instrument variability, all microperimeters were calibrated accurately by the same experienced technician, and the parameters of the examination were standardized at the 2 centers.

SD OCT images were obtained with the Spectralis OCT version 5.1.3.0 (Heidelberg Engineering, Heidelberg, Germany) with Heidelberg Eye Explorer version 1.6.2.0 (Heidelberg Engineering). At each center, all OCT examinations were carried out by a certified operator (M.Z., Catania; B.B., Rome) who was unaware of other information on the eyes. According to the protocol, radial 20-degree, 6-line scans centered on the fovea were obtained for each eye. More than 25 scans were averaged for each measurement. Only images with a quality score of more than 25 were selected as high-quality images. The integrity of the IS/OS and ELM was evaluated by using the photoreceptor IS/OS junction and ELM line on the gray-scale SD OCT images. Both the ELM line and the photoreceptor IS/OS junction were evaluated on each of the radial 6-line scans for 500 μm in either direction of the center of the fovea and were defined as intact when the line was continuous, disrupted when the line was interrupted by gaps shorter than 200 μm, or completely absent when the gaps were 200 μm or longer. On the basis of the appearance of 2 lines, 6 levels of integrity were described: VI, both the IS/OS junction and ELM line were intact; V, the IS/OS junction was disrupted, but the ELM line was intact; IV, the IS/OS junction was absent, but the ELM line was intact; III, both the IS/OS junction and the ELM line were disrupted; II, the IS/OS junction was absent and the ELM was disrupted; and I, both and the IS/OS junction and the ELM line were absent. According to the integrity of the foveal photoreceptor layer, the eyes were divided into 3 subgroups: group A, eyes with complete integrity of the IS/OS junction and the ELM line; group B, eyes with partial or complete disruption of the IS/OS junction with an intact ELM line; and group C, eyes with disruption of the ELM line. Two masked expert investigators at each center (M.R., A.L., Catania; M.V., M.P., Rome) interpreted the SD OCT images. When there was disagreement, a third investigator was consulted for the final decision.

Results

Sixty eyes of 60 consecutive patients with a diagnosis of LMH were evaluated; of these, 6 eyes were excluded (2 for other macular disease, 2 for refractive error more than ± 5 diopters, 1 for significant cataract, and 1 for previous vitrectomy). Therefore, 54 eyes of 54 patients met the study criteria and were enrolled. The demographic and clinical characteristics of the enrolled patients are reported in Table 1 . High-quality SD OCT scans were obtained for each patient, and none were eliminated from the study secondary to inability to grade the photoreceptor layer. The ICC between observers for the grading of the IS/OS junction was 0.96 (95% confidence interval [CI], 0.92 to 0.97), and the ICC between observers for the status of the ELM line was 0.82 (95% CI, 0.70 to 0.89). The κ coefficient for the status of the IS/OS junction was 0.91 (95% CI, 0.78 to 1.03) and that for the status of the ELM line was 0.81 (95% CI, 0.56 to 1.07).

At SD OCT examination, 40 eyes (74%) showed complete integrity of the IS/OS junction and ELM line, whereas 14 eyes (26%) had alterations in the photoreceptor layer: in detail, 7 eyes (13%) had a disrupted IS/OS junction with an intact ELM line, 1 (2%) had a completely absent IS/OS junction with an intact ELM line, 2 (4%) had disrupted IS/OS junction and ELM line, 4 (7%) had an absent IS/OS junction and disrupted ELM line; no eye had a completely absent ELM line. Spearman regression analysis showed that the degree of integrity of the photoreceptor layer was correlated significantly with BCVA ( r = −0.57; P < .001), total retinal sensitivity ( r = 0.44; P = .001), and central retinal sensitivity ( r = 0.52; P < .001), but not with fixation stability ( P = not significant).

Table 2 shows the subgroup analysis of groups A, B, and C according to the integrity of the photoreceptor layer. Mean BCVA, mean central retinal sensitivity, mean total retinal sensitivity, and mean fixation stability were significantly different among the 3 groups. For mean BCVA, mean total retinal sensitivity and mean fixation stability, the values for groups A and B were significantly higher than that for group C ( P < .05, Tukey–Kramer test), whereas there was no significant difference between groups A and B ( P = not significant). The mean central retinal sensitivity in groups A and B was significantly higher than that in group C ( P < .001, Tukey–Kramer test), and that in group A was significantly higher than that in group B ( P < .05, Tukey–Kramer test; Figure 1 ). Examples of OCT and microperimetry findings of the patients in the groups A, B, and C are displayed in Figure 2 .

TABLE 2

Difference in Best-corrected Visual Acuity, Retinal Sensitivity, and Fixation Stability among Eyes with Various Levels of Photoreceptor Integrity Detected by Spectral-Domain Optical Coherence Tomography in Eyes with Lamellar Macular Holes

	Photoreceptor Layer Integrity			P Value
	Eyes with Preserved IS/OS and ELM: Group A (n = 40)	Eyes with Disrupted IS/OS and Preserved ELM: Group B (n = 8)	Eyes with Disrupted IS/OS and ELM: Group C (n = 6)	ANOVA	Tukey–Kramer
BCVA, logMAR	0.08 ± 0.05	0.13 ± 0.09	0.30 ± 0.11	.000	NS a
					.000 b c
Total sensitivity, dB	17.7 ± 1.5	16.7 ± 2.5	13.1 ± 2.4	.000	NS a
					.001 b
					.000 c
Central sensitivity, dB	17.1 ± 2	15 ± 3	10.5 ± 2.4	.000	.047 a
					.001 b
					.000 c
Fixation stability, %	92 ± 8	91 ± 11	78 ± 16	.006	NS a
					.039 b
					.004 c

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