Purpose
To investigate the correlation of microperimetry with fundus autofluorescence (FAF), spectral-domain optical coherence tomography (SD-OCT), and visual acuity (VA) in order to better characterize visual outcomes after successful macular hole (MH) surgery.
Design
Cross-sectional case series.
Methods
Postoperative VA, microperimetry, FAF, and SD-OCT images from 23 eyes of 23 patients who underwent successful MH surgery were obtained. FAF images were examined using the Heidelberg retina angiograph 2, and foveal structure and macular sensitivity were evaluated with SD-OCT and microperimetry. The mean retinal sensitivities within the central 9 degrees (microperimetry, mean), the retinal sensitivity of the foveal center (microperimetry, center), and the difference between the values obtained for the foveal center or mean of study and fellow eyes (microperimetry, centerdiff and microperimetry, meandiff, respectively) were measured with microperimetry.
Results
Microperimetry (mean) was well correlated with microperimetry (center) in both study and fellow eyes. Poor postoperative VA was correlated with large microperimetry (meandiff). Following successful MH surgery, FAF of all eyes decreased markedly. There was a positive correlation between microperimetry (centerdiff) and degree of FAF of study eyes. However, a decrease in FAF after MH surgery was not correlated well with either degree of defect in the junction between photoreceptor inner and outer segment (IS/OS) or central retinal thickness on SD-OCT.
Conclusions
The amount of remaining FAF is related to macular sensitivity as measured by microperimetry after successful MH surgery. Function of photoreceptors and retinal pigment epithelium as well as integrity can be estimated by measuring the decrease in FAF after successful MH surgery. Moreover, functional correlation with microperimetry provides both morphologic and functional information on repaired MHs.
Idiopathic full-thickness macular hole is an important cause of central vision impairment in the elderly. Since Kelly and Wendel first reported on surgical correction of macular hole (MH), anatomic closure of MHs has been achieved in most cases. However, complete closure of MH as confirmed by optical coherence tomography (OCT) does not always result in good visual recovery. There also have been conflicting results reported regarding the postoperative visual acuity (VA) in relation to several preoperative variables such as the size of MH, duration of MH existence, or preoperative VA. Complete closure of MH does not always imply that the function of the neurosensory retina is recovered, which should be closely related to the postoperative VA. Villate and associates suggested that certain specific structural features within the foveal architecture may be more important than others to restore visual function in patients with closed MH. Recently, the appearance of the photoreceptor layer in OCT has been reported to be correlated with good VA after successful MH surgery. Spectral-domain OCT (SD-OCT) enhances the resolution with which the intraretinal architectural morphology, especially the photoreceptor layer, is viewed. With this improvement in the resolution of SD-OCT, the junction between photoreceptor inner and outer segment (IS/OS) can be clearly seen. The presence of the IS/OS indicates normal alignment of the photoreceptors, and this alignment is essential for normal visual function. Poor postoperative recovery of photoreceptor morphology (typically misalignment of the discs in the outer segments) was suggested to be 1 reason for an unfavorable visual prognosis among long-standing MH cases.
However, even IS/OS morphology assessed by SD-OCT may not precisely reflect the postoperative functional visual gain. Chang and associates reported that the improvement in VA was not correlated with the change in the size of the IS/OS defect after MH repair. In surgically repaired retinal detachment, VA was not always correlated with findings on SD-OCT.
Recently, a new technique of in vivo imaging of the fundus autofluorescence (FAF), which is most likely derived from lipofuscin in the retinal pigment epithelium (RPE), has been used to measure the function and morphology of the retina and RPE in various diseases such as age-related macular degeneration (AMD) or retinal dystrophy. In fovea, there was local hypofluorescence, which was probably attributable in part to absorption of short-wavelength light by macular pigment including lutein and zeaxanthin. FAF findings of full-thickness macular hole (FTMH) described bright (increased) autofluorescence (AF) because there is no overlying masking macular pigment. von Rückmann and associates also reported that FAF of the MHs was no longer visible following successful surgical treatment, while there was a persistent increased AF after unsuccessful surgery. The bright AF disappeared after MH closure, because the RPE was again covered by retinal and/or glial tissue, as demonstrated also by OCT images.
While FAF is an indirect measure to assess the function and/or morphology of the retina and the RPE, microperimetry can directly analyze retinal sensitivity in certain specific points on the macula. Microperimetry has been successfully used in the diagnosis and follow-up of different macular disorders including MH. Microperimetry findings highlight the value of functional macula mapping for these patients and indicate that the functional benefit of surgical repair is underestimated when compared with testing VA alone.
In the present study, we found that patients showed variable degrees of remaining FAF even after complete closure of MH. Therefore, we investigated the relationships among microperimetry, FAF, SD-OCT findings, and VA to better characterize visual outcomes after successful MH surgery. The characteristics of FAF in relation to the morphologic (SD-OCT) and functional (microperimetry, VA) outcomes of surgically repaired MHs were evaluated.
Methods
We followed 23 patients (2 men and 21 women) who underwent surgery for idiopathic FTMHs between January 1, 2008 and September 30, 2008. The patient age ranged from 45 to 71 years (mean, 61 years). Patients with bilateral MHs or any diseases involving macula at the fellow eyes were excluded from this study. Microincision vitrectomy (23- or 25-gauge) and internal limiting membrane peeling with indocyanine green (0.05%) staining was performed. No attempt was made to aspirate over and around the MH. Cataract surgery was combined in 21 eyes. Vitrectomy alone was performed in 2 pseudophakic eyes. At the end of the vitrectomy, air was replaced by a mixture of air and C 3 F 8 (8%). After surgery, patients were asked to hold their heads in a face-down position for 1 week. All patients underwent best-corrected visual acuity (BCVA) measurements, both SD-OCT imaging of the macula and macular microperimetry by Spectral OCT/SLO (OTI, Toronto, Canada), and FAF imaging using the Heidelberg retina angiograph 2 (HRA2, Heidelberg, Germany) at an average of 10 months after MH surgery. The scan acquisition protocols for SD-OCT imaging include 5-line raster scans and a macular cube 200 × 200 Combo. The macular cube 200 × 200 Combo consists of a horizontal 200 A-scans measured to 200 vertical lines across an area of 6 × 6 mm. Thirty-μm slices were examined in both horizontal and vertical directions. The amount of IS/OS defects on SD-OCT was graded as none, focal, small, or diffuse (or invisible) by 3 retinal surgeons who operated in a masked manner. In the microperimetry test, a Goldmann III size stimulus was used, and 25 stimulus locations covering the central 9 degrees were examined by microperimetry. The duration of the stimulus was 200 ms (flashing test stimuli measuring 5 × 5 pixels were presented for 200 ms by a helium-neon laser). The retinal sensitivity at the center of the fovea (microperimetry, center) and the mean retinal sensitivities at 24 locations covering the central 9 degrees of both study and fellow eyes were determined. The mean retinal sensitivities within the central 9 degrees (microperimetry, mean), the retinal sensitivity of the foveal center (microperimetry, center), and the difference in the retinal sensitivity of the foveal center or the mean of the study and the fellow eyes (microperimetry, centerdiff and microperimetry, meandiff, respectively) were measured with microperimetry.
As the amount of fluorescent light (at approximately 500 nm) emitted by the RPE is extremely low, an confocal scanning laser ophthalmoscope. (HRA2; Heidelberg, Germany) was used with both exciter illumination and barrier filters in place. The degrees of FAF were subjectively graded (grade 1-4) independently by the same retina surgeons. These values were compared with those obtained using the semiautomatic method by an expert (J.K.K.), using Matlab (MathWorks) for Wiener filtering, thresholding, and analyzing images ( http://www.mathworks.com/products/matlab ). Briefly, step 1 was cropping the region of interest (ROI) in each FAF image, because we are interested in the variation of brightness around the macula. This excludes the effect of a transparency in the tissue, vessel, etc. Step 2 was enhancement of the signal-to-noise ratio in tissue by Wiener filter. The Wiener filter is applied to ROI images. Step 3 was expert-aided segmentation of the images. Because the brightness of FAF in a healthy eye is likely to decrease monotonically toward the center of the macula (foveola), a local bright segment will be problematic. Thus, the threshold value was adjusted until the resulting boundary and the expert-subjective boundary were almost similar. Then, the resulting binary image for a local bright segment was trimmed to form a single image. Step 4 was calculation of the representative value of local bright segments. The value was defined by the area multiplied by the mean, where area is the size of a local bright segment and mean is the average value of brightness of local bright segment (ie, value = (A1 × B1) + (A2 × B2) + …).
The SPSS V14.0 software program (SPSS Inc., Chicago, Illinois, USA) was used for all statistical analyses, and P value < .05 was considered as statistically significant. The possible correlations between variables were investigated using the Spearman rank correlation test.
Results
All 23 patients showed complete closure of MH, defined clinically by an ophthalmoscopic and SD-OCT examination. The mean Snellen VA of the 23 study eyes improved from 20/200 preoperatively to 20/50 postoperatively. The mean VA in logMAR significantly improved from 1.02 to 0.44 ( P < .001). The average value of microperimetry (mean) of the study and fellow eyes was 8.89 (standard deviation, 2.16) and 10.95 (standard deviation, 2.18), respectively. The average value of microperimetry (center) of the study and fellow eyes was 6.96 (standard deviation, 4.23) and 8.68 (standard deviation, 3.29), respectively. Microperimetry (mean) was well correlated with microperimetry (center) in both study and fellow eyes (r 2 = 0.716, P < .001; r 2 = 0.704, P = .001, respectively). Poor preoperative VA was correlated with lower postoperative microperimetry (mean) and microperimetry (center) of the study eyes (r 2 = −0.521, P = .027; r 2 = −0.514, P = .029, respectively). The poorer the preoperative VA, the lower the postoperative microperimetry threshold. Poor postoperative VA was also correlated with large microperimetry (meandiff) (r 2 = 0.486, P = .035). The poorer the postoperative VA, the larger the difference with respect to the nondiseased eyes ( Figure 1 ).
Following successful closure of MH after surgery, the FAF of all eyes decreased markedly. There were 10 eyes that were graded 1, 6 eyes graded 2, 3 eyes graded 3, and 4 eyes graded 4. The subjectively graded amount of FAF was well correlated with the semiautomatic method ( Supplemental Figure 1 , available at AJO.com ) using an image analyzer (r = 0.889, P < .001) ( Figure 2 ). There was a positive correlation between microperimetry (centerdiff) and the degree of FAF in the study eyes (r = 0.469, P = .037) ( Figure 3 ). In other words, the FAF of the study eyes tended to be high when there were large differences between the retinal sensitivities of the foveal centers of the study eyes and normal fellow eyes. However, preoperative and postoperative VA (logMAR) and time after surgery were not correlated with FAF. The extent of the IS/OS defect on SD-OCT was graded as none, focal, small, or diffuse (or invisible) ( Figure 4 ). Six eyes were graded as none, 7 eyes were graded as focal, 8 eyes were graded as small, and 2 eyes were graded as diffuse defect. The mean central macular thickness in eyes with repaired MHs as determined by SD-OCT machine was 240.3 μm (standard deviation, 31.6). A decrease in FAF after successful MH surgery was not correlated with either the degree of IS/OS defects or central macular thickness on SD-OCT. The postoperative degree of IS/OS defects was not correlated with the preoperative and postoperative VA (logMAR) or measured microperimetry parameters. Study eyes with focal IS/OS defects had good visual outcomes (logMAR), as did eyes with intact IS/OS seen on SD-OCT (0.379 ± 0.212 vs 0.333 ± 0.137, P = .663) ( Figure 5 ).
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