Asymmetry of Optic Nerve Head Parameters Measured by Confocal Scanning Laser Ophthalmoscopy in Myopic Anisometropic Eyes
Joint Shantou International Eye Center, Shantou University and the Chinese University of Hong Kong, Shantou 515041, China
*
Author to whom correspondence should be addressed.
Appl. Sci. 2022, 12(8), 4047; https://doi.org/10.3390/app12084047
Submission received: 9 March 2022
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Revised: 12 April 2022
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Accepted: 13 April 2022
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Published: 16 April 2022
(This article belongs to the Special Issue Application and Prospect of Optical-Related Imaging Technology in Biomedical Imaging)
Abstract
:Background: This study aimed to evaluate the asymmetry of optic nerve head parameters measured by confocal scanning laser ophthalmoscopy (CSLO) in myopic anisometropic eyes. Methods: A total of 36 eyes of 18 healthy myopic anisometropic subjects, defined as cases in which the difference in spherical equivalent (SE) between both eyes is ≥1.5D, were recruited. The optic nerve heads were measured using the Heidelberg retina tomograph II (Heidelberg Engineering, GmBH, Heidelberg, Germany). Differences in optic nerve head parameters between more myopic eyes and fellow eyes were evaluated using the paired-sample t-test. Pearson correlation and multiple linear regression analysis were used to evaluate factors associated with cup/disc ratio (CDR). Results: The cup/disc area ratio (mean difference 0.07 ± 0.11, P = 0.027), horizontal (mean difference 0.10 ± 0.17, P = 0.033), and vertical CDR (mean difference 0.13 ± 0.18, P = 0.008) were significantly smaller in more myopic eye. Larger disc area was independently and significantly associated with larger cup/disc area ratio (β = 0.561, P = 0.001) and vertical CDR (β = 0.499, P = 0.03). Conclusion: The CDR, horizontal, and vertical CDR were significantly smaller in the more myopic eyes in myopic anisometropic subjects. Further studies with larger samples are needed to confirm the asymmetry of the optic nerve head in myopic anisometropic eyes.
1. Introduction
Glaucoma is the most common cause of irreversible blindness [1]. Patients with early glaucoma are usually asymptomatic. Early diagnosis is essential to prevent irreversible damage to the optic nerve [2,3,4,5]. To date, investigation of the optic nerve head plays an important role in the diagnosis of glaucoma. An increase in cup/disc ratio (CDR) and asymmetry of CDR between both eyes are important clinical findings of glaucoma [6,7,8,9].
Myopia is a worldwide common ocular disorder and is well known to be related to glaucoma [10,11]. Previous studies have shown that CDR is significantly correlated with the degree of myopia. Anisometropia is the condition in which the refractive errors of both eyes have significant differences. It is important to clarify whether anisometropia can cause asymmetry of CDR between both eyes in myopic patients. The Heidelberg retina tomograph (HRT; Heidelberg Engineering GmbH, Heidelberg, Germany) is a confocal scanning laser ophthalmoscope that acquires three-dimensional tomographic images of the ONH. It has been shown to be a useful technique to study the morphology of the optic nerve head, with a high degree of discrimination between healthy and glaucomatous eyes [12]. Some studies have reported no significant interocular difference in HRT-measured ONH parameters, whereas others have reported small but significant differences in normal subjects [13,14,15]. However, most of the studies focused on a healthy population with all types of refractive errors. Since myopia is an important risk factor for glaucoma, it would be valuable to perform a study to clarify the inter-eye differences in CDR in myopic anisometropia. To our knowledge, no study has used HRT to study the inter-eye difference in CDR in myopic anisometropia. Therefore, the purpose of this study is to evaluate the inter-eye asymmetry of CDR in myopic patients with anisometropia.
2. Materials and Methods
2.1. Ethical Approval
The study was designed following the ethical standards of the Declaration of Helsinki and approved by the Ethics Committee (EC 20111223(6)-P06) of the Joint Shantou International Eye Center (JSIEC), with written informed consent obtained before the study.
2.2. Subjects
In total, 18 Chinese subjects with inter-eye differences in spherical equivalent (SE) of more than 1.50D were recruited for our study, from June 2009 to November 2013. The SE for both eyes of each subject was ≤0.00D. All subjects received complete ophthalmic examinations, which included visual acuity, intraocular pressure (IOP), refraction, and axial length (AL) measured by IOL Master (Carl Zeiss Meditec Inc., Jena, Germany), as well as dilated fundus stereoscopic examination. The more myopic eyes of each subject were selected as the more myopic eye group, while the other eyes were selected as the less myopic eye group.
2.3. Inclusion and Exclusion Criteria
All of the included eyes had a spherical equivalent of less than 0.00D and no other concurrent diseases. Subjects with best-corrected visual acuity of less than 20/40, IOP over 21 mmHg, family history of glaucoma, intraocular surgery, myopic macular degeneration, clinical evidence of glaucoma, refractive surgery, age less than 18, neurological diseases, or diabetes were excluded.
2.4. Visual Field Testing
All visual field tests were performed with the static automated white-on-white threshold 24-2 SITA standard strategy (Humphrey Field Analyzer II; Carl Zeiss Meditec, Inc.). A visual field test was considered to be reliable when fixation loss, false-positive, and false-negative results were all less than 20%. All visual field tests of included eyes were within normal limits or with a general reduction in sensitivity in the glaucoma hemifield test (GHT).
2.5. HRT Imaging
The parameters of ONH were measured with confocal scanning laser ophthalmoscopy (Heidelberg retina tomograph II (HRT2); Heidelberg Engineering, GmbH, Dossenheim, Germany). In brief, HRT uses the technology of confocal scanning laser ophthalmoscope to acquire a series of scans of ONH. The 3-dimensional tomographic image of the ONH was reconstructed based on the scan images. Only the images with standard deviations of less than 30 μm were used in this study. The disc contour lines for all subjects were determined by one experienced operator (KL.Q.). The measurements of ONH were automatically generated by the software integrated into the machine. The standard reference plane is defined as 50 μm posterior to the mean retinal height between 350 and 356 degrees along the contour line.
2.6. Statistical Analysis
The statistical analyses were performed with commercially available software (SPSS ver. 13.0; SPSS Inc, Chicago, IL, USA). Paired t-test was used to compare the optic nerve head parameter between both eyes of each subject. Pearson correlation was used to evaluate the correlations between inter-eye differences in ONH parameters and SE/AL. Multiple linear regression analysis was used to evaluate the factors associated with cup/disc area ratio, vertical CDR, and horizontal CDR. P < 0.05 was considered statistically significant.
3. Results
A total of 36 eyes from 18 subjects meeting our inclusion criteria were included in this study. Eighteen eyes had astigmatism of less than 0D. Mean astigmatism for all eyes was −0.56 ± 0.76D (range: 0 to −3D). A significant difference in SE and AL (all P < 0.001) was found in both eyes. No significant difference was found in age, sex, and inter-eye difference in SE. The characteristics of the subjects were presented in Table 1.
3.1. Comparisons of ONH Parameters between Both Eyes Measured with HRT
The cup area in the more myopic eye was significantly smaller than that of the fellow eye (P = 0.032). The values in the more myopic eye were significantly smaller than those of the fellow eye in the measurements of cup/disc area ratio, linear CDR, horizontal CDR, and vertical CDR (all P < 0.05). No significant difference between both eyes was found in the measurement of disc area and rim area. Detailed information is shown in Table 2.
3.2. Correlations between Inter-Eye Differences in ONH Parameters and SE/AL
Inter-eye differences in cup/disc area ratio, horizontal CDR, vertical CDR, and linear CDR were all positively correlated with the inter-eye difference in AL, respectively. A positive correlation was also found between the inter-eye difference in SE and inter-eye difference in cup/disc area ratio, horizontal CDR, vertical CDR, and linear CDR, respectively. Both inter-eye differences in cup area and disc area were significantly correlated with inter-eye differences in AL and SE. The inter-eye difference in rim/disc area ratio was also found to be negatively correlated with the inter-eye differences in AL and SE. No significant correlation was found between the inter-eye difference in rim area and the inter-eye difference in AL/SE. Detailed information is shown in Table 3.
3.3. Factors Associated with Cup/Disc Ratio Parameters
Table 4 presents the multiple linear regression analysis regarding the associations between various factors and cup/disc area ratio, vertical CDR, and horizontal CDR. A larger disc area was independently and significantly associated with a larger cup/disc area ratio and vertical CDR. No significant association was found between SE/AL and the three-cup/disc ratio parameters. Table 5 presents the multiple linear regression analysis regarding the associations between inter-eye differences in various factors and inter-eye differences in cup/disc area ratio, vertical CDR, and horizontal CDR. The inter-eye difference in vertical CDR was positively correlated with the inter-eye difference in AL using the inter-eye difference in disc area as a covariate in a regression model. No significant association was found between the inter-eye difference in AL and the inter-eye difference in the other two cup/disc ratio parameters.
4. Discussion
In the current study, we found significant inter-eye differences in the cup area, cup/disc area ratio, linear CDR, horizontal CDR, and vertical CDR in anisometropic myopic subjects using HRT. Moreover, significant correlations were found between inter-eye differences in ONH parameters and inter-eye differences in AL/SE in terms of cup/disc area ratio, rim/disc area ratio, horizontal CDR, vertical CDR, and linear CDR. Inter-eye differences in cup and disc areas were also found to be significantly correlated with the inter-eye difference in AL. A larger disc area was independently and significantly associated with a larger cup/disc area ratio and vertical CDR. The inter-eye difference in vertical CDR was positively correlated with the inter-eye difference in AL using the inter-eye difference in disc area as a covariate in a regression model.
In the current study, all of the CDR parameters, including horizontal, vertical, lineal CDR, and cup/disc area ratio were smaller in the more myopic eyes in anisometropic subjects. The Rim/disc area ratio was larger in the more myopic eyes. No significant difference in rim area was found between both eyes. A previous study by Qiu et al. suggested that vertical CDR asymmetry could be useful to identify patients with a higher risk to develop glaucoma [16]. They found that the population-weighted 50th, 97.5th, and 99.5th percentiles of vertical CDR asymmetry were 0.05, 0.19, and 0.26, respectively in the US population. The current study included 18 healthy Chinese subjects with inter-eye differences in spherical equivalent (SE) of more than 1.50D (range: 1.50–3.88 D). The mean difference in vertical CDR was 0.13 ± 0.18. Although the mean difference in vertical CDR fell within the 97.5th percentile, the standard deviation was as large as 0.18. A considerable number of subjects (5 out of 18 subjects) were outside the normal range regarding vertical CDR. As CDR asymmetry is one of the parameters that raises suspicion of glaucoma, some otherwise healthy anisometropic patients with myopia might be considered glaucoma suspects because of asymmetric CDR.
The current study found that all inter-eye differences in cup/disc area ratio, horizontal CDR, vertical CDR, and linear CDR were positively correlated with the inter-eye difference in AL and SE. Regarding the correlation between optic disc parameters and refractive error/AL, previous studies had inconsistent results. Jonas et al. and Wang et al. found no correlation between optic disc size and refractive error within the range of −8D to +4D based on optic disc photographs [17,18]. In contrast, Ramrattan et al. suggested a negative correlation between optic disc area and refractive error based on optic disc photographs [19]. Leung et al. found that the optic disc area was correlated with AL/refractive error using HRT III [20]. In the same study, when only subjects within the range of −8D to +4D were analyzed, no correlation was found between optic disc area and refractive error/AL. Abe et al. also found a weak correlation between disc area and refractive error based on HRT [13]. Thus, the correlation between optic disc parameters and refractive error might not have been clinically relevant. In the current study, the range of refractive error was from −8D to 0D (mean: −4.17 ± 2.27D). The difference in disc area between the two eyes was not statistically significant. However, the inter-eye difference in the disc area increased as the inter-eye difference in refractive error/AL increased. Inter-eye differences in CDRs also increased as the inter-eye difference in refractive error/AL increased. We further evaluated the influences of AL, SE, and disc area on the measurement of cup/disc ratio parameters with the multiple linear regression analysis. A larger disc area was independently and significantly associated with a larger cup/disc area ratio and vertical CDR. No significant association was found between SE/AL and the cup/disc ratio parameters. The asymmetry of CDR might be caused by the asymmetry of the disc area between the eyes in myopic anisometropia. Since disc area was found to be correlated with cup/disc ratio parameters and AL, the inter-eye difference in disc area was used as a covariate in a regression model to evaluate the correlation between the inter-eye difference in AL and inter-eye differences in cup/disc ratio parameters. Among the cup/disc ratio parameters, only the inter-eye difference in vertical CDR was found to be positively correlated with the inter-eye difference in AL. The asymmetry of CDR could not be simply explained by the difference in refractive error between both eyes. As the inter-eye difference in refractive error increases, the asymmetry of CDR between two eyes may affect the diagnosis of glaucoma.
Several limitations exist in the present study. One potential limitation is the relatively small sample size of our study cohort. As both eyes from the same subjects were analyzed using paired t-test, the results still showed statistical significance with relatively small sample size. Further study with larger sample size is needed to confirm our results. In the present study, the mean age was 23.63 years (95% CI 21.02 to 26.24, range: 18 to 42). This is not the common range of age for POAG. As symmetry of CDR is important for early diagnosis of glaucoma, the results of the present study can be applied to the screening of POAG in young patients.
5. Conclusions
In summary, anisometropic myopic eyes may have asymmetric optic disc parameters, including CDRs. This may have an influence on the early diagnosis of POAG in such patients. Further studies with other refractive errors, different ages, and populations are warranted to further our understanding of the influence of anisometropia on the diagnosis of POAG.
Author Contributions
Conceptualization, G.W. and W.G.; methodology, G.W., X.L., and W.G.; formal analysis, G.W.; investigation, X.L. and W.G.; resources, W.G.; data curation, G.W. and W.G.; writing—original draft preparation, G.W. and W.G.; writing—review and editing, G.W.; supervision, G.W.; project administration, G.W.; funding acquisition, G.W. All authors have read and agreed to the published version of the manuscript.
Funding
This study was funded by the Guangdong Medical Research Foundation (CN) (Grant No A2016514), Shantou Municipal Science and Technology Project (Grant No 190917155269927), 2020 Li Ka Shing Foundation Cross-Disciplinary Research Grant (Project Number: 2020LKSFG06B).
Institutional Review Board Statement
The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee (EC 20111223(6)-P06) of the Joint Shantou International Eye Center (JSIEC).
Informed Consent Statement
Informed consent was obtained from all subjects involved in the study.
Data Availability Statement
The excel data used to support the findings of this study is available from the corresponding author upon request.
Acknowledgments
Abstract of the manuscript was presented as a poster at the 2017 ARVO Annual Meeting, held in Baltimore, MD, 7–11 May. Posterboard Number: 4006-A0315.
Conflicts of Interest
The authors declare no conflict of interest.
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Table 1.
Characteristics of the study subjects.
| More Myopic Eye Group (n = 18) | Less Myopic Eye Group (n = 18) | P # | |
|---|---|---|---|
| SE (diopters, mean ± SD) | −5.15 ± 1.81 | −2.95 ± 1.94 | <0.001 |
| Inter-eye difference in SE (diopters, mean ± SD) | 2.20 ± 0.62 | 2.20 ± 0.62 | |
| AL (mm, mean ± SD) | 25.37 ± 1.38 | 24.52 ± 1.29 | <0.001 |
| Age (years, mean ± SD) | 23.63 ± 5.25 | 23.63 ± 5.25 | |
| Sex (n female/n male) | 8/10 | 8/10 |
# Paired t-test. AL: axial length; SE: spherical equivalent.
Table 2.
Inter-eye comparisons of ONH parameters (paired t-test).
| More Myopic Eye Group (n = 18) | Less Myopic Eye Group (n = 18) | Mean Inter-Eye Difference | P | |
|---|---|---|---|---|
| Cup area (mm2, mean ± SD) | 0.37 ± 0.30 | 0.52 ± 0.32 | 0.14 ± 0.26 | 0.032 |
| Cup/disc area ratio (mean ± SD) | 0.17 ± 0.10 | 0.24 ± 0.11 | 0.07 ± 0.11 | 0.027 |
| Disc area (mm2, mean ± SD) | 1.96 ± 0.52 | 2.07 ± 0.57 | 0.11 ± 0.34 | 0.194 |
| Horizontal CDR (mean ± SD) | 0.45 ± 0.16 | 0.55 ± 0.13 | 0.10 ± 0.17 | 0.033 |
| Rim/disc area ratio (mean ± SD) | 0.83 ± 0.10 | 0.76 ± 0.11 | 0.07 ± 0.11 | 0.027 |
| Vertical CDR (mean ± SD) | 0.26 ± 0.15 | 0.39 ± 0.17 | 0.13 ± 0.18 | 0.008 |
| Linear CDR (mean ± SD) | 0.40 ± 0.12 | 0.47 ± 0.12 | 0.07 ± 0.13 | 0.025 |
| Rim area (mm2, mean ± SD) | 1.59 ± 0.32 | 1.55 ± 0.40 | 0.04 ± 0.22 | 0.505 |
ONH: optic nerve head. CDR: cup/disc ratio.
Table 3.
Correlations between inter-eye differences in ONH parameters and SE/AL (Pearson correlation).
Table 3.
Correlations between inter-eye differences in ONH parameters and SE/AL (Pearson correlation).
| Inter-Eye Difference in Parameters (Valueless myopic eye–Valuemore myopic eye) | Correlation with Inter-Eye Difference in AL(Valuemore myopic eye–Valueless myopic eye) r (P) (n = 18) | Correlation with Inter-Eye Difference in SE (Valueless myopic eye–Valuemore myopic eye) r (P) (n = 18) |
|---|---|---|
| Inter-eye difference in cup area | 0.61 (0.008) | 0.60 (0.009) |
| Inter-eye difference in cup/disc area ratio | 0.57 (0.014) | 0.61 (0.007) |
| Inter-eye difference in disc area | 0.48 (0.043) | 0.49 (0.041) |
| Inter-eye difference in horizontal CDR | 0.48 (0.043) | 0.56 (0.016) |
| Inter-eye difference in rim/disc area ratio | −0.57 (0.014) | −0.61 (0.007) |
| Inter-eye difference in vertical CDR | 0.60 (0.009) | 0.62 (0.006) |
| Inter-eye difference in linear CDR | 0.56 (0.017) | 0.62 (0.007) |
| Inter-eye difference in rim area | 0.02 (0.939) | 0.04 (0.887) |
AL: axial length; SE: spherical equivalent. CDR: cup/disc ratio.
Table 4.
Factors associated with cup/disc area ratio, vertical CDR, and horizontal CDR (multiple linear regression analysis).
Table 4.
Factors associated with cup/disc area ratio, vertical CDR, and horizontal CDR (multiple linear regression analysis).
| Cup/Disc Area Ratio | Vertical CDR | Horizontal CDR | ||||
|---|---|---|---|---|---|---|
| β | P | β | P | β | P | |
| SE | 0.184 | 0.508 | 0.342 | 0.230 | 0.189 | 0.557 |
| AL | 0.126 | 0.450 | 0.281 | 0.330 | 0.083 | 0.799 |
| Disc area | 0.561 | 0.001 | 0.499 | 0.003 | 0.318 | 0.076 |
AL: axial length; SE: spherical equivalent. CDR: cup/disc ratio.
Table 5.
Factors associated with inter-eye differences in cup/disc area ratio, vertical CDR, and horizontal CDR (multiple linear regression analysis).
Table 5.
Factors associated with inter-eye differences in cup/disc area ratio, vertical CDR, and horizontal CDR (multiple linear regression analysis).
| Inter-Eye Difference in Cup/Disc Area Ratio | Inter-Eye Difference in Vertical CDR | Inter-Eye Difference in Horizontal CDR | ||||
|---|---|---|---|---|---|---|
| β | P | β | P | β | P | |
| Inter-eye difference in AL | 0.408 | 0.092 | 0.495 | 0.048 | 0.289 | 0.242 |
| Inter-eye difference in Disc area | 0.332 | 0.164 | 0.212 | 0.371 | 0.399 | 0.113 |
AL: axial length; CDR: cup/disc ratio.
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Gong, W.; Lu, X.; Wang, G. Asymmetry of Optic Nerve Head Parameters Measured by Confocal Scanning Laser Ophthalmoscopy in Myopic Anisometropic Eyes. Appl. Sci. 2022, 12, 4047. https://doi.org/10.3390/app12084047
AMA Style
Gong W, Lu X, Wang G. Asymmetry of Optic Nerve Head Parameters Measured by Confocal Scanning Laser Ophthalmoscopy in Myopic Anisometropic Eyes. Applied Sciences. 2022; 12(8):4047. https://doi.org/10.3390/app12084047
Chicago/Turabian StyleGong, Weifen, Xuehui Lu, and Geng Wang. 2022. "Asymmetry of Optic Nerve Head Parameters Measured by Confocal Scanning Laser Ophthalmoscopy in Myopic Anisometropic Eyes" Applied Sciences 12, no. 8: 4047. https://doi.org/10.3390/app12084047
APA StyleGong, W., Lu, X., & Wang, G. (2022). Asymmetry of Optic Nerve Head Parameters Measured by Confocal Scanning Laser Ophthalmoscopy in Myopic Anisometropic Eyes. Applied Sciences, 12(8), 4047. https://doi.org/10.3390/app12084047
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