C L I N I C A L I N V E S T I G A T I O N
Foveal sensitivity and visual acuity in macular thickening disorders
Nami Chiba• Mitsuhiro Imasawa•Teruhiko Goto • Masahito Imai• Hiroyuki Iijima
Received: 29 September 2011 / Accepted: 27 February 2012 / Published online: 11 April 2012 ÓJapanese Ophthalmological Society 2012
Abstract
Purpose To study the relationship between foveal sensi- tivity and visual acuity in eyes with macular disorders exhibiting macular thickening.
Methods We studied the relationship between foveal sensitivity, obtained as the ‘‘foveal threshold’’ by use of Humphrey perimetry, and best-corrected visual acuity, converted to the logarithm of the minimum angle of reso- lution (logMAR), for 117 eyes with epiretinal membrane (ERM), 197 eyes with retinal vein occlusion associated with macular edema (RVOME), and 158 eyes with central serous chorioretinopathy (CSC).
Results Foveal sensitivity and logMAR correlated sig- nificantly for the eyes with ERM, RVOME, and CSC.
Although mean foveal sensitivity was no different among the three diseases, mean logMAR was lower in eyes with CSC, i.e., visual acuity was better, than in those with ERM or RVOME (P\0.001).
Conclusions Light sense (foveal sensitivity) is related to spatial resolution (logMAR) at the center of the fovea, in eyes with ERM, RVOME, and CSC at different strengths depending on the disease. Less pronounced reduction of visual acuity compared with foveal sensitivity in eyes with CSC could explain the tendency of these patients to com- plain of dimness rather than acuity loss.
Keywords Foveal sensitivityCentral serous chorioretinopathyRetinal vein occlusion Epiretinal membraneHumphrey perimetry
Introduction
Humphrey perimetry, the most common type of automated static perimetry, is used clinically in the management of ocular diseases, including glaucoma, neuro-ophthalmolog- ical disorders, and retinal diseases. In addition to measur- ing the sensitivity profile of the posterior pole of the retina in either a 30° or 10° area, Humphrey perimetry also provides a foveal threshold, which is the threshold of light sense at the fovea against a constant background lumi- nance. Because the sensitivity is the inverted value of the threshold, i.e., the minimum stimulus that evokes sensa- tion, and the foveal threshold in Humphrey perimetry is actually an inverted value of the measured threshold, with higher values representing lower threshold or higher sen- sitivity, it should be described as foveal sensitivity [1].
Flaxel et al. [2] report that few clinical studies use foveal sensitivity in Humphrey perimetry as a measure of foveal function [3–5]. They studied foveal sensitivity and best- corrected visual acuity converted to the logarithm of the minimum angle of resolution (logMAR) for 117 eyes with different eye conditions, including glaucoma and retinal diseases, and for normal subjects. Because they found that foveal sensitivity correlated highly with the logMAR, they concluded that foveal sensitivity could be used as a pre- dictor of the best-corrected visual acuity [2].
We also used foveal sensitivity to evaluate foveal function [6] and developed the clinical impression that the relationship between foveal sensitivity and best-corrected visual acuity is different among ocular diseases. For example, for patients with central serous chorioretinopathy (CSC), who tend to complain of dimness in the central field of vision [7], foveal sensitivity is often lower than for those with other macular diseases with equivalent logMAR.
Although both foveal sensitivity and logMAR are measures N. ChibaM. ImasawaT. GotoM. ImaiH. Iijima (&)
Department of Ophthalmology, Faculty of Medicine, University of Yamanashi, 1110 Shimokato, Chuo, Yamanashi 409-3898, Japan
e-mail: [email protected] DOI 10.1007/s10384-012-0137-4
of visual function of the fovea, the former, which repre- sents the threshold of luminance, may be different from the latter, which indicates the threshold of spatial dimension of minimum resolvable figures [8,9].
In this study, we investigated the relationship between foveal sensitivity and logMAR for three common macular disorders with different mechanisms of macular thickening, including epiretinal membrane (ERM), central or branch retinal vein occlusion with macular edema (RVOME), and CSC.
Methods
We retrospectively reviewed results from Humphrey perimetry (HFA 640 or HFA2-750; Humphrey Instruments, San Leandro, CA, USA) obtained for eyes with ERM, RVOME, and CSC at the department of Ophthalmology, University of Yamanashi Hospital, between January 1992 and September 2008. The foveal sensitivity, which is dis- played as the ‘‘foveal threshold’’ in Humphrey perimetry, was measured before either the Humphrey central 30-2 or 10-2 program. The patient was guided by the ‘‘small dia- mond’’ fixation lights, and a test stimulus light with a size of 4 mm2and duration of 0.2 ms was used. The best-cor- rected decimal visual acuity measured on the same day was converted to the logMAR.
Subjects
Epiretinal membrane was diagnosed by the characteristic macular finding of translucent membranes associated with various degrees of the tortuosity of the retinal vessels. We only included patients with ERM who later underwent vitrectomy.
Eyes with RVOME included 71 eyes with central retinal vein occlusion (CRVO) and 126 eyes with branch retinal
vein occlusion (BRVO) with reduced vision because of macular edema. Eyes with apparent areas of capillary nonperfusion around the fovea in a fluorescein angiogram were excluded from the study to preclude dysfunction because of macular ischemia. Those with massive retinal hemorrhage that obscured the retinal vessels in the macula were also excluded. We included eyes with optic disc vasculitis [10], a variant of CRVO seen in young subjects.
Data were obtained within 180 days of the initial symp- toms in all cases. In cases undergoing laser photocoagu- lation or vitreous surgery, data obtained before the treatment were studied.
The eyes with CSC were those in the active stage, with angiographic signs of dye leakage. Those of patients older than 59 years and those with angiographic signs of RPE atrophy or multiple dye leakage in the macula were not included. If the patient underwent laser photocoagulation, the foveal sensitivity and logMAR data obtained immedi- ately before the laser treatment were studied. All data were obtained within 60 days after onset of symptom of CSC, in both initial and recurrent cases.
We excluded cases with ocular diseases with visual dysfunction other than ERM, RVOME, and CSC; e.g., clinically significant cataract, glaucoma, diabetic retinop- athy, and corneal opacity. The demographic and clinical characteristics of the three categories of diseases are shown in Table1.
The study was approved by the University of Yamanashi Hospital ethics committee.
Statistics
LogMAR and foveal sensitivity in the three diseases were compared by analysis of variance (ANOVA). If significant, multiple comparisons were conducted by use of the Games–Howell pairwise comparison test. The correlations
Table 1 Subject characteristics and their logMAR and foveal sensitivity ERM
(n=117)
RVOME (n=197)
CSC (n=158)
Pvalue
Mean age±SD (range) 69±8 (40 to 86) 61±14 (16 to 89) 45±7 (27 to 59) \0.001*
Female/male 69/48 109/88 20/138 \0.001**
Mean logMAR±SD (range) 0.465±0.304
(-0.08 to 1.40)
0.428±0.382 (-0.18 to 1.70)
0.177±0.261 (-0.18 to 1.40)
\0.001*
Mean foveal sensitivity±SD (range) 27.6±5.5 (7 to 40) 26.4±6.9 (0 to 39) 27.4±6.6 (0 to 37) 0.206*
Spearman’s correlation coefficient between foveal sensitivity and logMAR
-0.428 (P\0.001***) -0.682 (P\0.001***) -0.392 (P\0.001***)
SDstandard deviation,logMARlogarithm of the minimum angle of resolution,ERMepiretinal membrane,CSCcentral serous chorioretinopathy, RVOMEretinal vein occlusion with macular edema
* Analysis of variance (ANOVA)
** Chi-squared test
*** Linear regression analysis
between logMAR and foveal sensitivity were tested by linear regression analysis.Pvalues of less than 0.05 were considered statistically significant. Statistical analysis was conducted by use of IBM SPSS statistics (version 19.0;
SPSS, Chicago, IL, USA).
Results
Mean age was significantly younger and the female- to-male ratio was significantly smaller for patients with CSC than for those with the other two diseases (Table1). Although mean foveal sensitivity was no dif- ferent among the three diseases, mean logMAR was statistically different (P\0.001, ANOVA). Compared with eyes with ERM or RVOME, logMAR was signifi- cantly lower for eyes with CSC (P\0.001, Games–
Howell pairwise comparison test). The decimal acuity
values corresponding to the mean logMAR in Table1 were 0.35 for ERM, 0.37 for RVOME, and 0.66, for CSC.
Foveal sensitivity correlated significantly with logMAR for each of the three diseases, with Spearman correlation coefficients between-0.392 and-0.682. The relationship between logMAR and foveal sensitivity for the three dis- eases is shown in Fig.1a–c. Note that the regression line for CSC is located below those for ERM and RVOME (Fig.1d) demonstrating that logMAR is significantly lower for eyes with CSC than for those with ERM and RVOME with equivalent foveal sensitivity.
Discussion
Foveal function is commonly evaluated by use of logMAR, the threshold of spatial resolution, i.e., the smallest letter
Fig. 1 Relationship between logMAR and foveal sensitivity for eyes with ERMa, RVOMEb, and CSCc. Thesize of each dotis weighted according to the respective number of cases, with the larger dots indicating more eyes.dThe regression lines for the three diseases.
ERM epiretinal membrane, RVOME retinal vein occlusion with macular edema, CSC central serous chorioretinopathy, logMAR logarithm of the minimum angle of resolution,dBdecibel
size that can be identified. Foveal sensitivity, which is obtained during examination with Humphrey perimetry, is another important foveal function evaluating light sense.
The results in this study reveal that these two measures of visual function at the fovea correlate with each other dif- ferently in the three macular disorders. However, the relationship did not seem to be identical among the dis- eases. The Spearman’s correlation coefficient between foveal sensitivity and logMAR was 0.68 for eyes with RVOME, which was equivalent to the results reported by Flaxel et al. [2] for eyes with diseases including glaucoma and several macular diseases. On the other hand, the cor- relation was not as strong for eyes with either ERM or CSC, for which correlation coefficients were approxi- mately 0.4.
Although most dots in the scatter plot for RVOME in Fig.1b were distributed around the regression line, indi- cating equal damage of both foveal sensitivity and log- MAR, the dots in the range of logMAR around zero in the scatter plot for CSC in Fig.1c were distributed in a broad range of foveal sensitivities from 10 to 35 decibels (dB), which means that, even with almost normal logMAR, eyes with CSC may have far lower foveal sensitivity than expected from good visual acuity. This may coincide with the clinical impression that many patients with CSC com- plain of dimness in the central visual field, despite normal visual acuity.
The regression lines between the foveal sensitivity and logMAR were located differently among the three diseases (Fig.1d), especially between CSC and either RVOME or ERM. The regression line for eyes with CSC was below those for eyes with either ERM or RVOME across almost the full range of foveal sensitivity. Visual acuity for the eyes with CSC was better than expected from the rela- tionships between foveal sensitivity and logMAR for eyes with either RVOME or ERM, which suggests, conversely, that for eyes with CSC foveal sensitivity is more damaged than visual acuity.
Although retinal thickening of the macula is common to all three diseases, the underlying mechanism is different among them. For eyes with ERM, thickening of the retina in the macula is a result of traction caused by contraction of the proliferative membrane adherent to the inner surface of the neural retina [11,12]. For eyes with RVOME including both BRVO and CRVO, for which there was no statistical difference in either logMAR (0.395±0.337 for BRVO and 0.486±0.449 for CRVO,P=0.138) or foveal sen- sitivity (26.8±6.7 for BRVO and 25.6±7.4, for CRVO, P=0.231), elevated intravenous pressure because of venous occlusion can cause extravasation of plasma com- ponents from the retinal circulation into the extracellular space in the neural retina, which may primarily damage conduction in the neural retina leading to visual
dysfunction [13,14]. On the other hand, leakage from the choroidal vessels into the subretinal space as a result of the reduced barrier function of the retinal pigment epithelium (RPE) is the chief mechanism for eyes with CSC, in which swelling of the neural retina is minimal [15]. Separation of the photoreceptors from the RPE by subretinal fluid con- taining plasma components may cause visual dysfunction by inhibiting renewal of the outer segment of the photoreceptors.
Foveal sensitivity is one visual function reflecting light sense or sensation of brightness which is primarily attrib- uted to the photoreceptors, whereas logMAR is another function defined by spatial resolution that depends on many factors other than the photoreceptors, including neural processing in the inner retina. Worse damage of light sense (foveal sensitivity) compared with the function of spatial resolution (logMAR) for eyes with CSC may reflect rela- tively selective damage in the photoreceptor cells them- selves in the fovea with minimal abnormality in their spacing or in neuroprocessing. The different relationship between foveal sensitivity and logMAR among the differ- ent macular diseases may result from different underlying pathological mechanisms in the photoreceptors and pro- cessing neurons.
This study has some limitations. First, the study was based on retrospective analysis. Second, the age and female-to-male ratios were different for subjects with CSC and the other two diseases. However, younger age and a higher number of men are inherent characteristics of CSC.
Some readers might be concerned about the poor fixation stability of the eyes with low visual acuity. We used only foveal sensitivity data measured using a fixation-aiding diamond of four lights, which resulted in far more reliable fixation than sensitivity measurements outside the fixation in ordinary Humphrey perimetry.
In conclusion, the two foveal functions logMAR and foveal sensitivity correlated with each other individually in the three macular diseases with macular thickening. The relationship between the two functions differed between the diseases evaluated; this is likely to reflect the under- lying pathophysiology of macular thickening.
Acknowledgments This study was supported in part by a Grant-in- Aid (no. 22591937) from the Ministry of Education, Science, Sports, and Culture, Japan. The authors indicate no financial conflicts of interest.
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