IOVS Journal of Applied Physiology
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(Investigative Ophthalmology and Visual Science. 2004;45:2224-2230.)
© 2004 by The Association for Research in Vision and Ophthalmology, Inc.
DOI:  10.1167/iovs.03-0297
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Retinal Nerve Fiber Layer Thickness in Unilateral Amblyopia

May-Yung Yen, Ching-Yu Cheng, and An-Guor Wang

From the Department of Ophthalmology, Taipei Veterans General Hospital, National Yang-Ming University, Taipei, Taiwan, Republic of China.


   Abstract
Top
 Abstract
Materials and Methods
 Results
 Discussion
 References
 
PURPOSE. To test the hypothesis that eyes with amblyopia may have thicker retina, retinal nerve fiber layer thickness (RNFLT) was investigated in patients with unilateral amblyopia.

METHODS. Thirty-eight patients with unilateral amblyopia were studied. Among them, 20 patients had amblyopia with strabismus and 18 had refractive amblyopia without strabismus. Nineteen of 38 had anisometropia of 2.0 D or more. In addition, 17 patients with anisometropia of 2.0 D or more but without amblyopia were enrolled as control subjects. RNFLT was measured by optical coherence tomography with scan pattern "Nerve Head 2.0R" (Carl Zeiss Meditec, Dublin, CA). Average RNFLT was multiplied with their corresponding scan circumferences to estimate the integral values of the total RNFL area (RNFLTestimated integrals).

RESULTS. In all 38 patients with unilateral amblyopia, the difference in RNFLT and in RNFLTestimated integrals between the amblyopic eyes and the normal fellow eyes were statistically significant. Multivariate regression analysis with adjustment for axial length, spherical equivalence, age, and sex indicated significant differences as well. In the group of strabismic amblyopia, the difference in RNFLT and in RNFLTestimated integrals between the amblyopic eyes and the normal fellow eyes did not reach statistical significance. However, in the group of refractive amblyopia, the difference in RNFLT and in RNFLTestimated integrals between the amblyopia eyes and the normal fellow eyes both had a statistical significance. In the 19 patients with anisometropic amblyopia, the difference in RNFLT and in RNFLTestimated integrals between the amblyopic eyes and the normal fellow eyes were statistically significant. In the control group of 17 patients with nonamblyopic anisometropia, the difference in RNFLT and in RNFLTestimated integrals between both eyes did not reach statistical significance.

CONCLUSIONS. RNFLT may be affected by refractive amblyopia, but further histopathologic confirmation is needed.

Amblyopia is considered to be a developmental disorder of spatial vision that is associated with the presence of strabismus, anisometropia, or form deprivation early in life.1 If the same disorders occur later in life, amblyopia does not develop.

The amblyopic process may have an effect on various levels of the visual pathway. Shrinkage of cells in the lateral geniculate nucleus that receive input from the amblyopic eye2 3 4 5 6 7 and a shift in the dominance pattern in the visual cortex8 9 10 11 12 have been reported. Retinal involvement accompanying amblyopia is controversial.13 14 15 16 17

During fetal development, there is a rapid decline in cell density in the retinal ganglion cell layer toward the end of gestation. In humans, the total population of cells in the ganglion cell layer is highest (2.2–2.5 million cells) between approximately weeks 18 and 30 of gestation. After this, the cell population declines rapidly to 1.5 to 1.7 million cells.18 The number of axons in the human optic nerve also decreases during gestation.19 At 16 to 17 weeks of gestation, the estimated number of axons was 3.7 million. The number of axons in the human adult optic nerve is 1.1 million. In rat retina, the number of retinal ganglion cells projecting to the central visual nuclei is reduced by at least 35%, and the process ceases by 2 weeks postnatally.20 If amblyopia affects the process of postnatal reduction of ganglion cells, RNFL thickness may be thicker than that in the normal eye. It was our plan to investigate retinal nerve fiber layer thickness (RNFLT) in amblyopic eyes to determine whether it is thicker.

Several techniques to evaluate the RNFLT, such as red-free ophthalmoscopy, scanning laser polarimetry (SLP) and optical coherence tomography (OCT) have been described. SLP estimates RNFLT based on the retardation of the laser beam caused by the birefringence of the RNFL. Because the cornea is also birefringent, erroneous RNFLT assessment can be made without proper anterior segment compensation.21 22 23 OCT is a noninvasive, noncontact technique that measures RNFLT.24 25 The RNFLT measured by OCT corresponds to the RNFLT measured histologically.24 Because OCT is based on near-infrared interferometry, the thickness measurement is not affected by refractive status or axial length of the eye, nor by light changes in nuclear sclerotic cataract density.26 RNFLT remains unchanged after laser-assisted in situ keratomileusis (LASIK).27 Posterior subcapsular and cortical cataracts, heavy nuclear cataracts, secondary cataracts, loss of vitreous body transparency, and silicone oil in the vitreous chamber, however, reduce the ability to perform OCT.26 28 Excluding these conditions, OCT is a reliable imaging technology. The purpose of our investigation was to use OCT to measure RNFLT in patients with unilateral amblyopia, to see whether the RNFL is thicker in the amblyopic eye.


   Materials and Methods
Top
 Abstract
 Materials and Methods
Results
 Discussion
 References
 
Subjects
Approval for this project was obtained from the institutional review board of Taipei Veterans General Hospital. The study was performed according to the tenets of the Declaration of Helsinki for research involving human subjects. Patients with unilateral amblyopia were consecutively enrolled. Clinical examinations included best corrected visual acuity, refraction error, slit lamp examination, extraocular movements, intraocular pressure, fundoscopy, and A-scan for axial length. Patients with organic eye disease, a history or evidence of intraocular surgery, history of cataract, glaucoma, retinal disorders, or laser treatment and children not cooperative enough for OCT examination were excluded.

A total of 38 patients with unilateral amblyopia were enrolled. Twenty had strabismic amblyopia (Table 1) . The other 18 without strabismus had a diagnosis of refractive amblyopia (Table 2) . Of the 38 patients with unilateral amblyopia, 19 also had anisometropia, including 7 from the group with strabismic amblyopia and 12 from the group with refractive amblyopia (Table 3) . Anisometropia was defined as a difference in spherical equivalence of 2.0 D or more between the two eyes. For the purpose of comparison, in addition, 17 patents with nonamblyopic anisometropia were enrolled as control subjects (Table 4) .


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  		TABLE 1. Basic Clinical Data of 20 Patients with Unilateral Amblyopia with Strabismus

 

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  		TABLE 2. Basic Clinical Data of 18 Patients with Refractive Amblyopia without Strabismus

 

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  		TABLE 3. Basic Clinical Data of 19 Patients with Amblyopia with Anisometropia

 

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  		TABLE 4. Basic Clinical Data of 17 Patients with Nonamblyopic Anisometropia

 
OCT Technique
After obtaining informed consent, the pupils were dilated with 1 drop of 1% tropicamide. RNFLT was measured by OCT 30 minutes later. The OCT system used in this study was OCT model 2000 (Carl Zeiss Meditec, Dublin, CA). The software version was 5.1. A peripapillary circular scan with scan pattern "Nerve Head 2.0R" was carefully positioned. The same scan pattern was used in all cases. Internal fixation was chosen unless the amblyopia was too deep to follow the fixation target. Average RNFLT detected by the circular scan was measured three times in each eye. Figure 1 showed a single OCT scan. All OCT measurements were performed by one of the authors (C-YC) who was not blind to the diagnosis. In every case, the right eye was always measured first, followed by the left eye.



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  		FIGURE 1. A single OCT scan of a normal eye.

 
Statistical Analysis
The mean of the three RNFLT measurement and RNFLTestimated integrals29 obtained from each eye were used for statistical analysis. Average RNFLT was multiplied with their corresponding scan circumferences to estimate the integral values of the total RNFL area: RNFLTestimated integrals (µm2) = RNFLTaverage (µm) x scan circumference (µm). Results are presented as mean ± SD. A paired Student’s t-test was used to assess the difference in RNFLT and in RNFLTestimated integrals between amblyopic and normal eyes in the patients with unilateral amblyopia and between both eyes of the patients with nonamblyopic anisometropia. P < 0.05 was considered to be statistically significant. To adjust for the possible effects of age, sex, refractive errors, and axial length on RNFL thickness, multivariate regression analysis was performed, and a generalized estimating equation30 was used to account for the correlation between both eyes in individuals. The correlation between RNFL thickness and other continuous variables was determined using Spearman’s rank correlation coefficient ({rho}).


   Results
Top
 Abstract
 Materials and Methods
 Results
Discussion
 References
 
Among 38 patients with unilateral amblyopia, 23 were male and 15 were female. The mean ± SD age was 26.4 ± 18.3 years. The eye with amblyopia was the right eye in 19 patients and the left eye in 19 patients. Best corrected vision of the amblyopic eye ranged from 20/1200 to 20/30. Best corrected vision of the normal eye was equal to or better than 20/20. The mean age of 20 patients with strabismic amblyopia was 27.4 ± 18.6 years, and the mean age of 18 patients with refractive amblyopia was 25.4 ± 18.6 years. The mean age of 17 normal control subjects was 28.5 ± 12.2 years.

In all 38 patients with unilateral amblyopia, the difference in RNFLT between the amblyopic eyes and the normal fellow eyes was statistically significant (Table 5) . The difference in RNFLTestimated integrals between the amblyopic eyes and the normal fellow eyes was also statistically significant (Table 6) . Multivariate regression analysis with adjustment for axial length, spherical equivalence, age, and sex indicated a significant difference in RNFLT and in RNFLTestimated integrals as well. Although the spherical equivalence in amblyopic eyes (0.17 ± 3.59 D) was higher than that in normal fellow eyes (–0.81 ± 2.33 D), the difference was not statistically significant (P = 0.084). In addition, there was no significant correlation between RNFLT and axial length ({rho} = –0.075, P = 0.655) or spherical equivalence ({rho} = –0.009, P = 0.956) among all amblyopic eyes. RNFLT in all amblyopic eyes did not correlate with logMAR visual acuity (P = 0.104) after adjustment for age.


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  		TABLE 5. Comparison of RNFL Thickness in Amblyopic and Normal Eyes

 

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  		TABLE 6. Comparison of RNFLTestimated integrals in Amblyopic and Normal Eyes

 
Further analysis was performed separately for strabismic and refractive amblyopia. In the group with strabismic amblyopia, the difference in RNFLT and RNFLTestimated integrals between the amblyopic eyes and the normal fellow eyes did not reach statistical significance. However, in the group of refractive amblyopia, the difference in RNFLT and in RNFLTestimated integrals between the amblyopic eyes and the normal fellow eyes were statistically significant (Tables 5 6) .

In the 19 patients with anisometropic amblyopia, the difference between RNFLT and RNFLTestimated integrals in the amblyopic eyes and in the normal fellow eyes both were statistically significant (Tables 5 6) . The differences were significant in the multivariate regression analysis as well. In the control group of 17 patients with nonamblyopic anisometropia, the difference in RNFLT and in RNFLTestimated integrals between the two eyes both did not reach statistical significance (Tables 7 8) .


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  		TABLE 7. Comparison of RNFL Thickness Between Eyes in Nonamblyopic Anisometropia

 

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  		TABLE 8. Comparison of RNFLTestimated integrals between Eyes in Nonamblyopic Anisometropia

 
Difference in RNFL thickness may come from glaucomatous damage and subjects older than 40 may confound the data analysis. Therefore, we also analyzed the data excluding subjects older than 40. The number of subjects was reduced to 31 from 38 (amblyopic) and to 13 from 17 (control). With a sample size of 31, the study had more than 80% statistical power to detect a 6% increase in RNFL thickness in amblyopic eyes, compared with the normal eyes. The results of RNFLT and RNFLTestimated integrals of the reduced number also consisted with the results of total number.


   Discussion
Top
 Abstract
 Materials and Methods
 Results
 Discussion
References
 
During an OCT examination, the selected preset scan radius is automatically modified by the instrument’s software. This modification is assumed to overcome the magnification produced by the patient’s eye. The actual projected scan radius was found to have statistically significant positive correlation with axial length.29 For each 1-mm increase in axial length, the actual projected scan radius increased approximately 0.06 mm or 3.5%. A final correction should be made by the examiner, by using a control knob, to reach the desired scan radius. This final correction of the actual projected scan radius, already modified by the instrument, should be made, especially in studies investigating the relationship of RNFL thickness measurement with axial length or refractive error. The study also found that theRNFLTestimated integrals area was found to be independent of the scan radius.29 We did not correct the actual radius when we performed the OCT examination. Therefore, we used two approaches to correct for this. First, we used multivariate regression analysis to adjust the effects of refractive errors and axial length on the measured RNFLT. Second, we used the "retinal nerve fiber layer total area" as a proxy parameter. Our study revealed RNFLT was thicker and RNFLTestimated integrals were larger in the amblyopic eye, especially in refractive amblyopia and in anisometropic amblyopia, but not in strabismic amblyopia.

The amblyopic process may have an effect on various levels of the visual pathway. Histopathologic changes in the lateral geniculate nucleus and visual cortex have been reported.

Histologic study of the lateral geniculate nucleus of monkeys with strabismic, anisometropic, and visual deprivation amblyopia reveals marked shrinkage of cells that receive input from the amblyopic eye.3 4 5 There are similar findings in the lateral geniculate nucleus in human anisometropic amblyopia6 and strabismic amblyopia.7

Wiesel and Hubel2 8 9 pioneered the application of microelectrode techniques to record directly from single neurons within the visual system of animals to study the effects of normal and abnormal visual experience early in life in visually immature kittens. Extracellular recordings from striate neurons in monkeys with strabismic, anisometropic, and visual deprivation amblyopia and in unilaterally lid-sutured kittens demonstrated a decimation of binocularly driven cells and of cells receiving input from the amblyopic eye.10 11 12 In humans, positron emission tomography scans revealed a significant reduction of relative cortical blood flow and glucose metabolism during visual stimulation of the amblyopic eye compared with the normal eye.31

Retinal involvement in strabismic and/or anisometropic amblyopia is controversial.13 14 15 16 17 Electroretinograms elicited by patterned stimuli in humans with various types of amblyopia were significantly reduced.13 The Stiles-Crawford effect or foveal visual pigment density, however, indicated no retinal dysfunction at the level of cone photoreceptors in amblyopic eyes.14 There have been no studies of either the anatomic or physiologic properties of the retina in monkeys reared with experimental amblyopia due to strabismus or anisometropia. Ikeda and Tremain15 reported that kittens reared with experimental esotropia had deficits in the spatial resolution of retinal ganglion cells in the area centralis of the deviating eye. Lid suture or surgical strabismus in cats, however, did not result in reduced ganglion cell resolution.16 17 In the present study, the RNFL thickness measured by OCT was significantly thicker in refractive amblyopia.

Using a third generation nerve fiber analyzer (GDx; Laser Diagnostic Technologies, San Diego, CA), Colen et al.32 measured RNFL thickness in strabismic amblyopia, and reported that there was no statistically significant difference between the strabismic amblyopic eyes and normal eyes. In the present study, RNFL thickness was not significantly different between strabismic amblyopic and normal eyes. However, the RNFL was thicker in refractive amblyopic eyes.

It is unclear why there is a difference in RNFL thickness between amblyopia associated with strabismus versus refractive error. Although strabismic and uncorrected refractive amblyopias are characterized by decreased visual acuity, psychophysical investigations33 34 35 revealed substantial differences in the visual characteristics of humans with different types of amblyopia. Using a vernier grating stimulus, anisometropic amblyopes show hyperacuity, while strabismic amblyopes show severe losses in vernier acuity. In addition, strabismic amblyopes show "crowding effects" for vernier gratings, while anisometropic amblyopes show no such effects. The findings suggest that different neural losses are associated with amblyopias of different etiologies. In our study, the RNFL was thicker and RNFLTestimated integrals were larger in eyes with refractive amblyopia, suggesting that the process of postnatal reduction of ganglion cells require sharply focused objects as appropriate stimuli.

In conclusion, in refractive amblyopia, there is a thicker RNFL. This finding requires further histopathologic confirmation.


   Footnotes
 
Supported by Grant 90-182 from Taipei Veterans General Hospital, Taipei, Taiwan.

Submitted for publication March 22, 2003; revised February 4 and March 9, 2004; accepted March 23, 2004.

Disclosure: M.-Y. Yen, None; C.-Y. Cheng, None; A.-G. Wang, None

The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Corresponding author: May-Yung Yen, Department of Ophthalmology, Taipei Veterans General Hospital, Taipei, 11217 Taiwan, ROC; myyen{at}vghtpe.gov.tw.


   References
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 Abstract
 Materials and Methods
 Results
 Discussion
 References
 

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