- Email: [email protected]
Binocular visual acuity interaction in children: summation and inhibition
Binocular visual acuity interaction in children: summation and inhibition Young Bok Lee, MD, Dong Gyu Choi, MD, PhD ABSTRACT ● Objective: To compare binocular visual acuity with the monocular visual acuity of the better eye and investigate the factors contributing to binocular interaction. Design: Retrospective observational study. Participants: We enrolled 332 children. They were divided into 3 groups according to binocular interaction: group A (binocular equivalency), group B (binocular summation), and group C (binocular inhibition). Methods: Monocular visual acuity, binocular visual acuity, and stereoacuity were evaluated. The main outcome measures were the prevalence rates of binocular interaction and factors associated with binocular interaction, including monocular visual acuity of the better eye, interocular difference of monocular visual acuity, and stereopsis. Results: Of 332 children, binocular summation and equivalency were noted in 218 (65.7%) and 95 (28.6%), respectively, and binocular inhibition in 19 (5.7%). The binocular visual acuity and monocular visual acuity of the better eye in group B were better than those in groups A and C, respectively (p ¼ 0.000). There was a significant correlation between monocular visual acuity of the better eye and binocular visual acuity in groups B and C (r ¼ 0.884, p ¼ 0.000; r ¼ 0.797, p ¼ 0.000, respectively). The interocular difference of monocular visual acuity in group B (0.05 ⫾ 0.07) was smaller than that in group C (0.13 ⫾ 0.06) (p ¼ 0.000). The proportion of children with good stereopsis was 74.3% in group B but only 31.6% in group C (p ¼ 0.001). Conclusions: About 66% of 332 patients had better binocular visual acuity than monocular visual acuity of the better eye. Our results suggest that the monocular visual acuity of the better eye, interocular difference of monocular visual acuity, and stereopsis affect binocular interaction.
Visual acuity (VA) assessment, one of the most common ophthalmologic examinations for detection of ocular disorders, is an important indicator of normal visual development. In clinical practice, monocular VA rather than binocular VA has been used to measure VA. However, in everyday life, people need both eyes to properly perceive objects. Binocular VA thus would be a particularly practical and useful parameter for evaluation of visual function. The human visual system combines monocular signals from both eyes to obtain binocular single vision.1 The quality of binocular vision is dependent on the degree of image similarity between the 2 eyes.1 Binocular interaction can be classified into 2 types: binocular summation and binocular inhibition.1 What is generally referred to as binocular summation is the phenomenon of binocular VA exceeding monocular VA of the better eye. Binocular inhibition, contrastingly, describes the state wherein binocular VA is inferior to the monocular VA of the better eye. Previous studies have demonstrated that vision with 2 eyes differs from that with 1 eye in VA, contrast sensitivity, and peripheral visual field.2–7 Limitations of these studies, however, included small sample numbers and exclusively Western populations. In this study, we estimated the prevalence rates of binocular summation and inhibition and explored multiple factors associated with binocular interaction.
METHODS Study Design
We retrospectively reviewed the medical records of 332 children (age range, 3–17 years) who visited our pediatric ophthalmology clinic between June and October 2013. Our study was approved by the Institutional Review Board of the Hallym University Medical Center (2014-01-07). All of the children had undergone ophthalmologic examinations, including monocular VA, binocular VA, stereoacuity, refractive error, and ocular alignment. The children were divided into 3 groups according to the binocular interaction: group A (binocular equivalency, logMAR binocular VA ¼ logMAR monocular VA of better eye), those who had the same value of acuity between binocular VA and monocular VA of better eye; group B (binocular summation, logMAR binocular VA o logMAR monocular VA of better eye), those who had better binocular VA than monocular VA of the better eye; group C (binocular inhibition, logMAR binocular VA 4 logMAR monocular VA of better eye), those who had worse binocular VA than monocular VA of the better eye. The exclusion criteria were as follows: (i) trauma, (ii) other ocular disease excepting strabismus, (iii) any history of ocular surgery, and (iv) any systemic disease such as Down syndrome or cerebral palsy.
& 2016 Canadian Ophthalmological Society. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jcjo.2016.07.012 ISSN 0008-4182/16 CAN J OPHTHALMOL — VOL. ], NO. ], ] 2016
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Binocular visual acuity interaction in children—Lee and Choi Ophthalmologic Examinations
The distant binocular and monocular VA were measured by Snellen VA chart on the first visit to our clinic. The binocular VA was recorded first to avoid disruption of fusion, and the monocular VA of each eye was examined randomly after occluding the contralateral eye with the subject’s spectacles (if any). For those children not wearing glasses on the first visit, VA without any refractive correction was measured and used for analysis. To avoid the learning effect, the examiner had the children read randomly chosen letters on the Snellen chart. We also determined the number of letters that the children read with both eyes compared with the better eye, whether more or less. Amblyopia was defined as an interocular VA difference of 2 lines or more. Cycloplegic refraction was performed with 1% cyclopentolate chloride, if needed. Anisometropia was defined as an interocular difference of 2.00 diopters or more in spherical equivalents. The angle of deviation was determined by the alternate prism cover test at distance and near (6 and 1/3 m) for all fields of gaze, using accommodative targets. The Krimsky method was used in several uncooperative children. For cooperative children, stereopsis was examined by Titmus Stereotest (Stereo Optical Co, Inc, Chicago, Ill.). Based on the degree of stereopsis, the children were divided into 3 groups: good (40–60 arcsec), fair (80–100 arcsec), and poor (4100 arcsec). Outcome Measures
The primary outcome measure was the prevalence rate of binocular interaction based on the binocular VA and monocular VA of the better eye. The secondary outcome measures were the binocular interaction index as well as the probable factors (including monocular VA of the better eye, interocular difference of monocular VA, and status of stereopsis) associated with binocular interaction. To obtain the binocular interaction index, we subtracted the monocular VA of the better eye from the binocular VA. We defined the interocular difference of monocular VA as the absolute difference between the 2 eyes. Statistical Analysis
The recorded VA was converted from decimal notation to logMAR units using the VA conversion chart for statistical analysis. The statistical analysis was performed with SPSS software, version 12.0K (SPSS Inc, Chicago, Ill.). The Kruskal–Wallis test and Fisher’s exact test were used to compare the values among the 3 groups. The associations were evaluated by Spearman’s correlation analysis. A p-value of o0.05 was considered to be statistically significant.
RESULTS A total of 332 children were included in this study: 165 (49.6%) boys and 167 (50.4%) girls. The mean age was
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Table 1—Demographic data on subjects Demographic characteristics Age (years) Sex (male/female), n Refractive type Myopia, n (%) Hyperopia, n (%) Emmetropia, n (%) Refractive error (diopters) Spherical equivalent Anisometropia, n (%) Amblyopia, n (%) Ocular alignment Orthotropia, n (%) Exotropia, n (%) Esotropia, n (%) Stereopsis by Titmus test (seconds of arc) Good, n (%) Fair, n (%) Poor, n (%) Monocular visual acuity (logMAR) of better eye Binocular visual acuity (logMAR) Binocular interaction Equivalency, n (%) Summation, n (%) Inhibition, n (%)
Total (N ¼ 332) 8.11 ⫾ 3.15 (range, 3–17) 165/167 166 (50.3) 83 (25.2) 81 (24.5) 1.12 ⫾ 2.93 (range, 9.00 to 7.50) 43 (13.0) 9 (2.7) 250 (82.7) 48 (15.8) 4 (1.5) 75.23 ⫾ 169.16 (range, 40–3000) 234 (70.4) 80 (24.1) 18 (5.5) 0.07 ⫾ 0.09 (range, 0–0.50) 0.02 ⫾ 0.10 (range, 0.10 to 0.52) 95 (28.6) 218 (65.7) 19 (5.7)
Emmetropia ¼ 0.50 diopters o spherical equivalent o þ0.50 diopters. Anisometropia ¼ interocular difference of refractive error in spherical equivalent Z2.00 diopters. Amblyopia ¼ interocular visual acuity difference Z2 lines. Stereopsis: Good (40–60 arcsec), Fair (80–100 arcsec), and Poor (4 100 arcsec). Binocular interaction: Equivalency (binocular visual acuity ¼ monocular visual acuity of better eye), summation (binocular visual acuity o monocular visual acuity of better eye), and inhibition (binocular visual acuity 4 monocular visual acuity of better eye).
8.11 ⫾ 3.15 years (range, 3–17 years). Anisometropia and amblyopia were observed in 43 (13.0%) and 9 (2.7%) children, respectively. The mean stereoacuity was 75.23 ⫾ 169.16 seconds of arc (range, 40–3000). Of the total of 332 children, 234 (70.4%), 80 (24.1%), and 18 (5.5%) showed good, fair, and poor stereopsis, respectively. The mean binocular VA and monocular VA of the better eye were 0.02 ⫾ 0.10 (range, 0.10 to 0.52) and 0.07 ⫾ 0.09 (range, 0–0.50), respectively. Binocular summation and equivalency were noted in 218 (65.7%) and 95 (28.6%) children, respectively, and binocular inhibition in 19 (5.7%). The demographic data are summarized in Table 1.
Monocular VA of Better Eye, Binocular VA, and Binocular Interaction Index According to Binocular Interaction
The mean monocular VA of the better eye was 0.08 ⫾ 0.08 in group A, 0.06 ⫾ 0.09 in group B, and 0.11 ⫾ 0.10 in group C (p ¼ 0.000, Kruskal–Wallis test) (Table 2). The mean binocular VA was 0.08 ⫾ 0.08 in group A, 0.00 ⫾ 0.08 in group B, and 0.14 ⫾ 0.11 in group C (p ¼ 0.001, Kruskal–Wallis test). Monocular VA of the better eye and binocular VA were better in group B than in group A and group C, respectively. The binocular interaction index was 0.07 logMAR in group B and 0.03
Binocular visual acuity interaction in children—Lee and Choi Table 2—Monocular visual acuity of better eye, binocular visual acuity, and binocular interaction index according to the binocular interaction
Monocular visual acuity of better eye Binocular visual acuity Binocular interaction index
Group A (n ¼ 95)
Group B (n ¼ 218)
Group C (n ¼ 19)
p
0.08 ⫾ 0.08 0.08 ⫾ 0.08 —
0.06 ⫾ 0.09 0.00 ⫾ 0.08 0.07 ⫾ 0.04
0.11 ⫾ 0.10 0.14 ⫾ 0.11 0.03 ⫾ 0.03
0.000* 0.001*
Group A: equivalency, binocular visual acuity ¼ monocular visual acuity of better eye. Group B: summation, binocular visual acuity o monocular visual acuity of better eye. Group C: inhibition, binocular visual acuity 4 monocular visual acuity of better eye. Binocular interaction index ¼ subtraction of monocular visual acuity from binocular visual acuity. n
Kruskal–Wallis test.
logMAR in group C. The children in group B read about 3 letters more with both eyes, whereas those in group C read 1 letter fewer. Factors Affecting Binocular Interaction
Table 3 compares the clinical factors according to binocular interaction. Among the 3 groups, there was no significant difference in any factor: age, sex, refractive error, amblyopia, anisometropia, or ocular alignment (p 4 0.05). Monocular VA of the better eye in group B was better than that in group C (p ¼ 0.000). There was a significant positive correlation between monocular VA of the better eye and binocular VA in groups B and C (r ¼ 0.884, p ¼ 0.000; r ¼ 0.797, p ¼ 0.000). The interocular difference of monocular VA in group B was smaller than that in group C (p ¼ 0.000). Accordingly, in group B, there was a negative correlation between the binocular interaction index and the interocular difference of monocular VA (r ¼ 0.545, p ¼ 0.000). Similarly, in group C, the interocular difference of monocular VA was correlated with the binocular interaction index (r ¼ 0.340, p ¼ 0.000).
Degree of Stereopsis According to Binocular Interaction
The mean stereoacuity was 95.87 ⫾ 309.68 seconds in group A, 65.19 ⫾ 46.48 seconds in group B, and 88.42 ⫾ 33.54 seconds in group C (p ¼ 0.327, Kruskal–Wallis test) (Table 4). The result was better for patients with binocular summation than in those with binocular inhibition, although the difference was not statistically significant (p ¼ 0.327). However, the proportion of children with good stereopsis was 68.5% in group A, 74.3% in group B, and 31.6% in group C (p ¼ 0.001, Fisher’s exact test).
DISCUSSION VA is an important indicator in the assessment of visual function. Thus, it is essential to evaluate it accurately. In clinical settings, ophthalmologists routinely obtain information on monocular VA; however, for performance of the activities of daily living, binocular VA is more important than monocular VA. In the present study, therefore, we evaluated binocular VA and determined
Table 3—Clinical factors affecting binocular interaction Group A (n ¼ 95) Age (years) Sex (male/female) Refractive type Myopia, n (%) Hyperopia, n (%) Emmetropia, n (%) Refractive error (diopters) Spherical equivalent Anisometropia, n (%) Amblyopia, n (%) Ocular alignment Orthotropia, n (%) Exotropia, n (%) Esotropia, n (%) Monocular visual acuity of better eye Interocular difference of monocular visual acuity
Group B (n ¼ 218)
Group C (n ¼ 19)
8.61 ⫾ 3.65 39/56
7.90 ⫾ 3.08 117/101
8.58 ⫾ 3.40 9/10
50 (52.6) 22 (23.2) 23 (24.2)
103 (47.2) 59 (27.1) 56 (25.7)
13 (68.4) 3 (15.8) 3 (15.8)
1.34 ⫾ 3.29 11 (11.6) 3 (3.2) 76 18 1 0.08 0.06
(80.0) (18.9) (1.1) ⫾ 0.08 ⫾ 0.06
1.07 ⫾ 3.10 32 (14.7) 5 (2.3) 188 27 3 0.06 0.05
(86.3) (12.4) (1.4) ⫾ 0.09 ⫾ 0.07
1.77 ⫾ 2.15 4 (21.1) 1 (5.3) 16 3 0 0.11 0.13
(84.2) (15.8) (0.0) ⫾ 0.10 ⫾ 0.06
p 0.244* 0.119† 0.466†
0.325* 0.519† 0.710† 0.282†
0.000* 0.000*
Group A: equivalency, binocular visual acuity ¼ monocular visual acuity of better eye. Group B: summation, binocular visual acuity o monocular visual acuity of better eye. Group C: inhibition, binocular visual acuity 4 monocular visual acuity of better eye. Emmetropia ¼ 0.50 diopters o spherical equivalent o þ0.50 diopters. Anisometropia ¼ interocular difference of refractive error in spherical equivalent Z2.00 diopters. Amblyopia ¼ interocular visual acuity difference Z2 lines. Interocular difference of monocular visual acuity ¼ absolute difference in monocular visual acuity between 2 eyes. n
†
Kruskal–Wallis test. Fisher’s exact test.
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Binocular visual acuity interaction in children—Lee and Choi Table 4—Comparison of stereopsis among 3 Groups
Mean stereoacuity (seconds of arc) Distribution of stereopsis Good, n (%) Fair, n (%) Poor, n (%) Group Group Group Good: n
†
Group A (n ¼ 95)
Group B (n ¼ 218)
Group C (n ¼ 19)
p
95.87 ⫾ 309.68
65.19 ⫾ 46.48
88.42 ⫾ 33.54
0.327* 0.001†
66 (69.5) 25 (26.3) 4 (4.2)
162 (74.3) 43 (19.7) 13 (6.0)
6 (31.6) 12 (63.2) 1 (5.3)
A: equivalency, binocular visual acuity ¼ monocular visual acuity of better eye. B: summation, binocular visual acuity o monocular visual acuity of better eye. C: inhibition, binocular visual acuity 4 monocular visual acuity of better eye. 40–60 arcsec, Fair: 80–100 arcsec, Poor: 4 100 arcsec.
Kruskal–Wallis test. Fisher’s exact test.
the differences and associations between monocular and binocular VA. The LALES Group reported that 21% of their study population presented binocular summation.8 By contrast, we observed binocular summation in 65.7% of the 332 patients in our study. The Salisbury Eye Evaluation Group, which examined a cohort of elderly people (aged 465 years), found a degree of summation of about 0.02 logMAR (1 letter on ETDRS chart), which was lower than that in our study (0.07 logMAR, 3 letters).9 The high prevalence and large degree of summation in the present study relative to the LALES and Salisbury Eye Evaluation Groups, respectively, were affected by our cohort’s young age. Gagnon and Kline reported that advanced age could be a factor impairing binocular summation.10 We also found that the age can affect the magnitude of binocular interaction. Indeed, the mean age of the children in our study was 8.14 years, which was markedly lower than those of the LALES (55.1 years) and Salisbury Eye Evaluation Group (465 years) subjects. This study, in a routine clinical setting, observed binocular inhibition in 19 (5.7%) of the child subjects. Walsh et al. found binocular inhibition in as many as 39.2% of their patients with intermittent exotropia.11 Similarly, according to the Pineles et al., binocular interaction was affected by the presence of strabismus.12 A possible explanation for this discrepancy between those previous reports and our study is the difference in the degree of ocular misalignment. In our study, ocular misalignment was observed only in 17.3% (n ¼ 52) of the children; moreover, the mean angle of deviation at distance was 11.38 ⫾ 5.59 PD in exotropia and 7.50 ⫾ 3.00 in esotropia, whereas in the study by Walsh et al., the mean exodeviation was 21.00 ⫾ 10.30 PD.11 In our opinion, the angle of deviation at distance in our study was too small to disrupt the stereopsis and thereby induce binocular inhibition; the presence of strabismus, therefore, did not become a significant factor influencing binocular interaction. Monocular VA of the better eye and binocular VA in group B were better than those in groups A and C, respectively. In groups B and C, a significant positive
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correlation between monocular VA of the better eye and binocular VA was observed (r ¼ 0.884 and r ¼ 0.797, respectively): The children with the better monocular VA had a better chance of manifesting binocular summation. Also, the interocular difference of monocular VA in the binocular summation group (group B) was smaller than that in the binocular inhibition group (group C). According to a Pearson correlation analysis moreover, in group B, there was a negative association between the binocular interaction index and the interocular difference of monocular VA (r ¼ 0.545, p ¼ 0.000), and the interocular difference of monocular VA in group C was negatively correlated with the binocular interaction index (r ¼ 0.340, p ¼ 0.000). In light of these correlations in the binocular summation and inhibition groups, it can be seen how binocular interaction would be affected by the interocular difference of monocular VA. In fact, the children with a small interocular difference of monocular VA appeared to have better binocular summation. The proportion of patients with good stereopsis was 74.3% in group B (binocular summation) and 31.6% in group C (binocular inhibition) (p ¼ 0.001). We may presume, then, that binocular interaction is associated with stereopsis, which is a marker of binocularity. In summary, monocular VA of better eye, interocular difference of VA, and stereopsis were considered to play important roles in binocular interaction. On that basis, we assumed that good monocular VA and stereopsis along with small interocular difference of VA are predictive factors for binocular summation. There are some limitations to this study. First, the mean age of the subjects was only 8.14 years. Some uncooperative preschool children tended to lose concentration in the assessment of VA and to stop looking at the figures on the VA chart. Thus, VA possibly was underestimated. Second, the child cohort, being quite small, was insufficient to draw any firm conclusions on the prevalence of binocular interaction. In conclusion, we found that about 66% of the total of 332 patients had better binocular VA than monocular VA. Monocular VA, interocular difference of VA, and stereopsis were found to be contributory factors to binocular interaction.
Binocular visual acuity interaction in children—Lee and Choi REFERENCES 1. Vedamurthy I, Suttle CM, Alexander J, Asper LJ. Interocular interactions during acuity measurement in children and adults, and in adults with amblyopia. Vis Res. 2007;47:179-88. 2. Cagnello R, Arditi A, Halpern DL. Binocular enhancement of visual acuity. J Opt Soc Am A. 1993;10:1841-8. 3. Home R. Binocular summation: a study of contrast sensitivity, visual acuity, and recognition. Vis Res. 1978;18:579-85. 4. Pradhan S, Elliott DB. Clinical measurements of binocular summation and inhibition in patients with cataract. Clin Vis Sci. 1991;6: 355-9. 5. Pradhan S. Binocular performances in patients with unilateral cataract using the Regan test: binocular summation and inhibition with low contrast charts. Eye. 1993;7:59-62. 6. Derefeldt FD, Lennerstrand G, Lundh B. Age variations in normal human contrast sensitivity. Acta Ophthalmol. 1979;57:679-90. 7. Pradhan S. A comparison of binocular summation in young and older patients. Curr Eye Res. 1996;15:315-9. 8. Azen SP, Varma R, Preston-Martin S, Ying-Lai M, Globe D, Hahn S. Binocular visual acuity summation and inhibition in an ocular epidemiological study: the Los Angeles Latino Eye Study. Invest Ophthalmol Vis Sci. 2002;43:1742-8. 9. Rubin GS, Munoz B, Bandeen-Roche K, West SK. Monocular versus binocular visual acuity as measures of vision impairment and predictors of visual disability. Invest Ophthalmol Vis Sci. 2000;41:3327-34.
10. Gagnon RW, Kline DW. Senescent effects on binocular summation for contrast sensitivity and spatial interval acuity. Curr Eye Res. 2003;27:315-21. 11. Walsh LA, Laroche GR, Tremblay F. The use of binocular visual acuity in the assessment of intermittent exotropia. J AAPOS. 2000;4:154-7. 12. Pineles SL, Velez FG, Isenberg SJ, et al. Functional burden of strabismus: decreased binocular summation and binocular inhibition. JAMA Ophthalmol. 2013;131:1413-9.
Footnotes and Disclosure: The authors have no proprietary or commercial interest in any materials discussed in this article. From the Department of Ophthalmology, Hallym University College of Medicine, Kangnam Sacred Heart Hospital, Seoul, Korea. Originally received Mar. 9, 2016. Accepted Jul. 28, 2016. Correspondence to Dong Gyu Choi, MD, PhD, Department of Ophthalmology, Hallym University College of Medicine, Kangnam Sacred Heart Hospital, 948-1 Daerim-dong, Youngdeungpo-gu, Seoul 150-950, Korea; [email protected]
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Visual acuity (VA) assessment, one of the most common ophthalmologic examinations for detection of ocular disorders, is an important indicator of normal visual development. In clinical practice, monocular VA rather than binocular VA has been used to measure VA. However, in everyday life, people need both eyes to properly perceive objects. Binocular VA thus would be a particularly practical and useful parameter for evaluation of visual function. The human visual system combines monocular signals from both eyes to obtain binocular single vision.1 The quality of binocular vision is dependent on the degree of image similarity between the 2 eyes.1 Binocular interaction can be classified into 2 types: binocular summation and binocular inhibition.1 What is generally referred to as binocular summation is the phenomenon of binocular VA exceeding monocular VA of the better eye. Binocular inhibition, contrastingly, describes the state wherein binocular VA is inferior to the monocular VA of the better eye. Previous studies have demonstrated that vision with 2 eyes differs from that with 1 eye in VA, contrast sensitivity, and peripheral visual field.2–7 Limitations of these studies, however, included small sample numbers and exclusively Western populations. In this study, we estimated the prevalence rates of binocular summation and inhibition and explored multiple factors associated with binocular interaction.
METHODS Study Design
We retrospectively reviewed the medical records of 332 children (age range, 3–17 years) who visited our pediatric ophthalmology clinic between June and October 2013. Our study was approved by the Institutional Review Board of the Hallym University Medical Center (2014-01-07). All of the children had undergone ophthalmologic examinations, including monocular VA, binocular VA, stereoacuity, refractive error, and ocular alignment. The children were divided into 3 groups according to the binocular interaction: group A (binocular equivalency, logMAR binocular VA ¼ logMAR monocular VA of better eye), those who had the same value of acuity between binocular VA and monocular VA of better eye; group B (binocular summation, logMAR binocular VA o logMAR monocular VA of better eye), those who had better binocular VA than monocular VA of the better eye; group C (binocular inhibition, logMAR binocular VA 4 logMAR monocular VA of better eye), those who had worse binocular VA than monocular VA of the better eye. The exclusion criteria were as follows: (i) trauma, (ii) other ocular disease excepting strabismus, (iii) any history of ocular surgery, and (iv) any systemic disease such as Down syndrome or cerebral palsy.
& 2016 Canadian Ophthalmological Society. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jcjo.2016.07.012 ISSN 0008-4182/16 CAN J OPHTHALMOL — VOL. ], NO. ], ] 2016
1
Binocular visual acuity interaction in children—Lee and Choi Ophthalmologic Examinations
The distant binocular and monocular VA were measured by Snellen VA chart on the first visit to our clinic. The binocular VA was recorded first to avoid disruption of fusion, and the monocular VA of each eye was examined randomly after occluding the contralateral eye with the subject’s spectacles (if any). For those children not wearing glasses on the first visit, VA without any refractive correction was measured and used for analysis. To avoid the learning effect, the examiner had the children read randomly chosen letters on the Snellen chart. We also determined the number of letters that the children read with both eyes compared with the better eye, whether more or less. Amblyopia was defined as an interocular VA difference of 2 lines or more. Cycloplegic refraction was performed with 1% cyclopentolate chloride, if needed. Anisometropia was defined as an interocular difference of 2.00 diopters or more in spherical equivalents. The angle of deviation was determined by the alternate prism cover test at distance and near (6 and 1/3 m) for all fields of gaze, using accommodative targets. The Krimsky method was used in several uncooperative children. For cooperative children, stereopsis was examined by Titmus Stereotest (Stereo Optical Co, Inc, Chicago, Ill.). Based on the degree of stereopsis, the children were divided into 3 groups: good (40–60 arcsec), fair (80–100 arcsec), and poor (4100 arcsec). Outcome Measures
The primary outcome measure was the prevalence rate of binocular interaction based on the binocular VA and monocular VA of the better eye. The secondary outcome measures were the binocular interaction index as well as the probable factors (including monocular VA of the better eye, interocular difference of monocular VA, and status of stereopsis) associated with binocular interaction. To obtain the binocular interaction index, we subtracted the monocular VA of the better eye from the binocular VA. We defined the interocular difference of monocular VA as the absolute difference between the 2 eyes. Statistical Analysis
The recorded VA was converted from decimal notation to logMAR units using the VA conversion chart for statistical analysis. The statistical analysis was performed with SPSS software, version 12.0K (SPSS Inc, Chicago, Ill.). The Kruskal–Wallis test and Fisher’s exact test were used to compare the values among the 3 groups. The associations were evaluated by Spearman’s correlation analysis. A p-value of o0.05 was considered to be statistically significant.
RESULTS A total of 332 children were included in this study: 165 (49.6%) boys and 167 (50.4%) girls. The mean age was
2
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Table 1—Demographic data on subjects Demographic characteristics Age (years) Sex (male/female), n Refractive type Myopia, n (%) Hyperopia, n (%) Emmetropia, n (%) Refractive error (diopters) Spherical equivalent Anisometropia, n (%) Amblyopia, n (%) Ocular alignment Orthotropia, n (%) Exotropia, n (%) Esotropia, n (%) Stereopsis by Titmus test (seconds of arc) Good, n (%) Fair, n (%) Poor, n (%) Monocular visual acuity (logMAR) of better eye Binocular visual acuity (logMAR) Binocular interaction Equivalency, n (%) Summation, n (%) Inhibition, n (%)
Total (N ¼ 332) 8.11 ⫾ 3.15 (range, 3–17) 165/167 166 (50.3) 83 (25.2) 81 (24.5) 1.12 ⫾ 2.93 (range, 9.00 to 7.50) 43 (13.0) 9 (2.7) 250 (82.7) 48 (15.8) 4 (1.5) 75.23 ⫾ 169.16 (range, 40–3000) 234 (70.4) 80 (24.1) 18 (5.5) 0.07 ⫾ 0.09 (range, 0–0.50) 0.02 ⫾ 0.10 (range, 0.10 to 0.52) 95 (28.6) 218 (65.7) 19 (5.7)
Emmetropia ¼ 0.50 diopters o spherical equivalent o þ0.50 diopters. Anisometropia ¼ interocular difference of refractive error in spherical equivalent Z2.00 diopters. Amblyopia ¼ interocular visual acuity difference Z2 lines. Stereopsis: Good (40–60 arcsec), Fair (80–100 arcsec), and Poor (4 100 arcsec). Binocular interaction: Equivalency (binocular visual acuity ¼ monocular visual acuity of better eye), summation (binocular visual acuity o monocular visual acuity of better eye), and inhibition (binocular visual acuity 4 monocular visual acuity of better eye).
8.11 ⫾ 3.15 years (range, 3–17 years). Anisometropia and amblyopia were observed in 43 (13.0%) and 9 (2.7%) children, respectively. The mean stereoacuity was 75.23 ⫾ 169.16 seconds of arc (range, 40–3000). Of the total of 332 children, 234 (70.4%), 80 (24.1%), and 18 (5.5%) showed good, fair, and poor stereopsis, respectively. The mean binocular VA and monocular VA of the better eye were 0.02 ⫾ 0.10 (range, 0.10 to 0.52) and 0.07 ⫾ 0.09 (range, 0–0.50), respectively. Binocular summation and equivalency were noted in 218 (65.7%) and 95 (28.6%) children, respectively, and binocular inhibition in 19 (5.7%). The demographic data are summarized in Table 1.
Monocular VA of Better Eye, Binocular VA, and Binocular Interaction Index According to Binocular Interaction
The mean monocular VA of the better eye was 0.08 ⫾ 0.08 in group A, 0.06 ⫾ 0.09 in group B, and 0.11 ⫾ 0.10 in group C (p ¼ 0.000, Kruskal–Wallis test) (Table 2). The mean binocular VA was 0.08 ⫾ 0.08 in group A, 0.00 ⫾ 0.08 in group B, and 0.14 ⫾ 0.11 in group C (p ¼ 0.001, Kruskal–Wallis test). Monocular VA of the better eye and binocular VA were better in group B than in group A and group C, respectively. The binocular interaction index was 0.07 logMAR in group B and 0.03
Binocular visual acuity interaction in children—Lee and Choi Table 2—Monocular visual acuity of better eye, binocular visual acuity, and binocular interaction index according to the binocular interaction
Monocular visual acuity of better eye Binocular visual acuity Binocular interaction index
Group A (n ¼ 95)
Group B (n ¼ 218)
Group C (n ¼ 19)
p
0.08 ⫾ 0.08 0.08 ⫾ 0.08 —
0.06 ⫾ 0.09 0.00 ⫾ 0.08 0.07 ⫾ 0.04
0.11 ⫾ 0.10 0.14 ⫾ 0.11 0.03 ⫾ 0.03
0.000* 0.001*
Group A: equivalency, binocular visual acuity ¼ monocular visual acuity of better eye. Group B: summation, binocular visual acuity o monocular visual acuity of better eye. Group C: inhibition, binocular visual acuity 4 monocular visual acuity of better eye. Binocular interaction index ¼ subtraction of monocular visual acuity from binocular visual acuity. n
Kruskal–Wallis test.
logMAR in group C. The children in group B read about 3 letters more with both eyes, whereas those in group C read 1 letter fewer. Factors Affecting Binocular Interaction
Table 3 compares the clinical factors according to binocular interaction. Among the 3 groups, there was no significant difference in any factor: age, sex, refractive error, amblyopia, anisometropia, or ocular alignment (p 4 0.05). Monocular VA of the better eye in group B was better than that in group C (p ¼ 0.000). There was a significant positive correlation between monocular VA of the better eye and binocular VA in groups B and C (r ¼ 0.884, p ¼ 0.000; r ¼ 0.797, p ¼ 0.000). The interocular difference of monocular VA in group B was smaller than that in group C (p ¼ 0.000). Accordingly, in group B, there was a negative correlation between the binocular interaction index and the interocular difference of monocular VA (r ¼ 0.545, p ¼ 0.000). Similarly, in group C, the interocular difference of monocular VA was correlated with the binocular interaction index (r ¼ 0.340, p ¼ 0.000).
Degree of Stereopsis According to Binocular Interaction
The mean stereoacuity was 95.87 ⫾ 309.68 seconds in group A, 65.19 ⫾ 46.48 seconds in group B, and 88.42 ⫾ 33.54 seconds in group C (p ¼ 0.327, Kruskal–Wallis test) (Table 4). The result was better for patients with binocular summation than in those with binocular inhibition, although the difference was not statistically significant (p ¼ 0.327). However, the proportion of children with good stereopsis was 68.5% in group A, 74.3% in group B, and 31.6% in group C (p ¼ 0.001, Fisher’s exact test).
DISCUSSION VA is an important indicator in the assessment of visual function. Thus, it is essential to evaluate it accurately. In clinical settings, ophthalmologists routinely obtain information on monocular VA; however, for performance of the activities of daily living, binocular VA is more important than monocular VA. In the present study, therefore, we evaluated binocular VA and determined
Table 3—Clinical factors affecting binocular interaction Group A (n ¼ 95) Age (years) Sex (male/female) Refractive type Myopia, n (%) Hyperopia, n (%) Emmetropia, n (%) Refractive error (diopters) Spherical equivalent Anisometropia, n (%) Amblyopia, n (%) Ocular alignment Orthotropia, n (%) Exotropia, n (%) Esotropia, n (%) Monocular visual acuity of better eye Interocular difference of monocular visual acuity
Group B (n ¼ 218)
Group C (n ¼ 19)
8.61 ⫾ 3.65 39/56
7.90 ⫾ 3.08 117/101
8.58 ⫾ 3.40 9/10
50 (52.6) 22 (23.2) 23 (24.2)
103 (47.2) 59 (27.1) 56 (25.7)
13 (68.4) 3 (15.8) 3 (15.8)
1.34 ⫾ 3.29 11 (11.6) 3 (3.2) 76 18 1 0.08 0.06
(80.0) (18.9) (1.1) ⫾ 0.08 ⫾ 0.06
1.07 ⫾ 3.10 32 (14.7) 5 (2.3) 188 27 3 0.06 0.05
(86.3) (12.4) (1.4) ⫾ 0.09 ⫾ 0.07
1.77 ⫾ 2.15 4 (21.1) 1 (5.3) 16 3 0 0.11 0.13
(84.2) (15.8) (0.0) ⫾ 0.10 ⫾ 0.06
p 0.244* 0.119† 0.466†
0.325* 0.519† 0.710† 0.282†
0.000* 0.000*
Group A: equivalency, binocular visual acuity ¼ monocular visual acuity of better eye. Group B: summation, binocular visual acuity o monocular visual acuity of better eye. Group C: inhibition, binocular visual acuity 4 monocular visual acuity of better eye. Emmetropia ¼ 0.50 diopters o spherical equivalent o þ0.50 diopters. Anisometropia ¼ interocular difference of refractive error in spherical equivalent Z2.00 diopters. Amblyopia ¼ interocular visual acuity difference Z2 lines. Interocular difference of monocular visual acuity ¼ absolute difference in monocular visual acuity between 2 eyes. n
†
Kruskal–Wallis test. Fisher’s exact test.
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Binocular visual acuity interaction in children—Lee and Choi Table 4—Comparison of stereopsis among 3 Groups
Mean stereoacuity (seconds of arc) Distribution of stereopsis Good, n (%) Fair, n (%) Poor, n (%) Group Group Group Good: n
†
Group A (n ¼ 95)
Group B (n ¼ 218)
Group C (n ¼ 19)
p
95.87 ⫾ 309.68
65.19 ⫾ 46.48
88.42 ⫾ 33.54
0.327* 0.001†
66 (69.5) 25 (26.3) 4 (4.2)
162 (74.3) 43 (19.7) 13 (6.0)
6 (31.6) 12 (63.2) 1 (5.3)
A: equivalency, binocular visual acuity ¼ monocular visual acuity of better eye. B: summation, binocular visual acuity o monocular visual acuity of better eye. C: inhibition, binocular visual acuity 4 monocular visual acuity of better eye. 40–60 arcsec, Fair: 80–100 arcsec, Poor: 4 100 arcsec.
Kruskal–Wallis test. Fisher’s exact test.
the differences and associations between monocular and binocular VA. The LALES Group reported that 21% of their study population presented binocular summation.8 By contrast, we observed binocular summation in 65.7% of the 332 patients in our study. The Salisbury Eye Evaluation Group, which examined a cohort of elderly people (aged 465 years), found a degree of summation of about 0.02 logMAR (1 letter on ETDRS chart), which was lower than that in our study (0.07 logMAR, 3 letters).9 The high prevalence and large degree of summation in the present study relative to the LALES and Salisbury Eye Evaluation Groups, respectively, were affected by our cohort’s young age. Gagnon and Kline reported that advanced age could be a factor impairing binocular summation.10 We also found that the age can affect the magnitude of binocular interaction. Indeed, the mean age of the children in our study was 8.14 years, which was markedly lower than those of the LALES (55.1 years) and Salisbury Eye Evaluation Group (465 years) subjects. This study, in a routine clinical setting, observed binocular inhibition in 19 (5.7%) of the child subjects. Walsh et al. found binocular inhibition in as many as 39.2% of their patients with intermittent exotropia.11 Similarly, according to the Pineles et al., binocular interaction was affected by the presence of strabismus.12 A possible explanation for this discrepancy between those previous reports and our study is the difference in the degree of ocular misalignment. In our study, ocular misalignment was observed only in 17.3% (n ¼ 52) of the children; moreover, the mean angle of deviation at distance was 11.38 ⫾ 5.59 PD in exotropia and 7.50 ⫾ 3.00 in esotropia, whereas in the study by Walsh et al., the mean exodeviation was 21.00 ⫾ 10.30 PD.11 In our opinion, the angle of deviation at distance in our study was too small to disrupt the stereopsis and thereby induce binocular inhibition; the presence of strabismus, therefore, did not become a significant factor influencing binocular interaction. Monocular VA of the better eye and binocular VA in group B were better than those in groups A and C, respectively. In groups B and C, a significant positive
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correlation between monocular VA of the better eye and binocular VA was observed (r ¼ 0.884 and r ¼ 0.797, respectively): The children with the better monocular VA had a better chance of manifesting binocular summation. Also, the interocular difference of monocular VA in the binocular summation group (group B) was smaller than that in the binocular inhibition group (group C). According to a Pearson correlation analysis moreover, in group B, there was a negative association between the binocular interaction index and the interocular difference of monocular VA (r ¼ 0.545, p ¼ 0.000), and the interocular difference of monocular VA in group C was negatively correlated with the binocular interaction index (r ¼ 0.340, p ¼ 0.000). In light of these correlations in the binocular summation and inhibition groups, it can be seen how binocular interaction would be affected by the interocular difference of monocular VA. In fact, the children with a small interocular difference of monocular VA appeared to have better binocular summation. The proportion of patients with good stereopsis was 74.3% in group B (binocular summation) and 31.6% in group C (binocular inhibition) (p ¼ 0.001). We may presume, then, that binocular interaction is associated with stereopsis, which is a marker of binocularity. In summary, monocular VA of better eye, interocular difference of VA, and stereopsis were considered to play important roles in binocular interaction. On that basis, we assumed that good monocular VA and stereopsis along with small interocular difference of VA are predictive factors for binocular summation. There are some limitations to this study. First, the mean age of the subjects was only 8.14 years. Some uncooperative preschool children tended to lose concentration in the assessment of VA and to stop looking at the figures on the VA chart. Thus, VA possibly was underestimated. Second, the child cohort, being quite small, was insufficient to draw any firm conclusions on the prevalence of binocular interaction. In conclusion, we found that about 66% of the total of 332 patients had better binocular VA than monocular VA. Monocular VA, interocular difference of VA, and stereopsis were found to be contributory factors to binocular interaction.
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Footnotes and Disclosure: The authors have no proprietary or commercial interest in any materials discussed in this article. From the Department of Ophthalmology, Hallym University College of Medicine, Kangnam Sacred Heart Hospital, Seoul, Korea. Originally received Mar. 9, 2016. Accepted Jul. 28, 2016. Correspondence to Dong Gyu Choi, MD, PhD, Department of Ophthalmology, Hallym University College of Medicine, Kangnam Sacred Heart Hospital, 948-1 Daerim-dong, Youngdeungpo-gu, Seoul 150-950, Korea; [email protected]
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