sign in sign up
<<
Home , Amblyopia, Refractive error

Original Article

Prevalence of Color Vision Deficiency and its Correlation with and Refractive Errors among Primary School Children

Zhale Rajavi1,2, MD; Hamideh Sabbaghi3,4, MS; Ahmad Shojaei Baghini4, MD; Mehdi Yaseri3,5, PhD Koroush Sheibani4, MD; Ghazal Norouzi6, MD 1Ophthalmic Epidemiology Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran 2Department of , Shahid Beheshti University of Medical Sciences, Tehran, Iran 3Ophthalmic Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran 4Basir Safety Research Center, Basir Eye Clinic, Tehran, Iran 5Department of Epidemiology and Biostatistics, Tehran University of Medical Sciences, Tehran, Iran 6School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Abstract Purpose: To determine the prevalence of color vision deficiency (CVD) and its correlation with amblyopia and refractive errors among primary school children. Methods: In this population‑based cross‑sectional study, 2160 children were selected from 36 primary schools; 60 students were from each school (10 students in each grade), with equal sex distribution. A complete including using a photorefractometer, determination of (VA) and color vision using a Yang vision tester, and evaluation of ocular media opacity using a direct ophthalmoscope was performed. Children who could not answer at least 4 plates of the Ishihara color test were considered as color vision deficient subjects. Amblyopia was determined if pinhole VA was worse than 0.3 LogMAR (equal to 20/40). Results: The prevalence of CVD was 2.2% (95% CI: 1.5% to 3%) which was higher in male subjects (37 [3.5%] boys vs. 11 [1.0%] girls, P < 0.001). Mean VA was lower among students with CVD as compared to normal color vision children (P = 0.035) and amblyopia was observed in 8.3% (95% CI: 0.2% to 16.4%) of patients with CVD versus 2.1% (95% CI: 1.5% to 2.08%) of children with normal color vision perception (P = 0.005). A statistically significant correlation between lower VA and CVD was observed (P = 0.023). Conclusion: Although CVD was correlated with lower VA and amblyopia, there was no relationship between CVD and the type of amblyopia, , or .

Keywords: Amblyopia; Color Vision Deficiency; Refractive Error; Visual Acuity

J Ophthalmic Vis Res 2015; 10 (2): 130-138.

Correspondence to: INTRODUCTION Hamideh Sabbaghi, MS. Ophthalmic Research Center, Shahid Beheshti University of Medical Sciences, No. 23, The prevalence of inherited red‑green color vision Paidarfard St., Boostan 9 St., Pasdaran Ave., deficiency (CVD) has been reported to be 8% and Tehran 16666, Iran. 0.4% in male and female individuals among European E‑mail: [email protected] Caucasian populations[1‑5] and 4% to 6.5% among male Received: 23-02-2014 Accepted: 17-11-2014 This is an open access article distributed under the terms of the Creative Commons Attribution‑NonCommercial‑ShareAlike 3.0 License, which allows Access this article online others to remix, tweak, and build upon the work non‑commercially, as long as the author is credited and the new creations are licensed under the identical terms. Quick Response Code: Website: www.jovr.org For reprints contact: [email protected]

How to cite this article: Rajavi Z, Sabbaghi H, Baghini AS, Yaseri M, DOI: Sheibani K, Norouzi G. Prevalence of color vision deficiency and its 10.4103/2008-322X.163778 correlation with amblyopia and refractive errors among primary school children. J Ophthalmic Vis Res 2015;10:130-8.

130 © 2015 Journal of Ophthalmic and Vision Research | Published by Wolters Kluwer - Medknow Color Vision Deficiency and Amblyopia;Rajavi et al subjects of Chinese origin.[5‑11] In Saudi Arabia, the rate of school (10 students in each grade). Available data from CVD in female individuals has been 0.35%.[12] A marked 2150 children was used in the final analysis; incomplete difference between male and female ratios has usually data from 10 other children was discarded due to different been testified.[5] reasons. Patients with mental retardation, ocular diseases Although decreased vision is the prominent sign of or anomalies and disorders of fixation were excluded. amblyopia,[13] there are certain associated microscopic The study was approved by the Ethics Committee anatomical and structural abnormalities in the ,[14,15] of the Ophthalmic Research Center, Shahid Beheshti lateral geniculate body (LGB)[15,16] and in area V1 of the University of Medical Sciences, Tehran, Iran and Basir .[15,17,18] Deficiency in other visual functions Eye Safety Research Center and adhered to the tenets of including sensitivity, binocularity, the crowding the Declaration of Helsinki. Formal written consent was phenomenon and visual evoked potential may be obtained from the students’ parents prior to the study. observed along with amblyopia.[19] The participants were interviewed by school health Patients affected with disorders such as optic instructors and a questionnaire concerning past health neuropathies, macular diseases, media opacities and history and demographic status of the subjects was filled, amblyopia show a higher prevalence of CVD; among then a complete eye examination including VA and color these, amblyopic children demonstrate the lowest vision assessment, refractive error measurement, ocular prevalence of CVD.[20] Color perception arises from deviation determination, anterior and posterior segments signals generated by three cone photoreceptors with evaluation and observation was performed. different spectral sensitivity functions. Signals from the retina which pass through the LGB are eventually Visual Acuity and Color Vision Testing transmitted to the cerebral cortex.[21] Transmission of We used the Yang vision tester (SIFI Diagnostic S.P.A‑Via color and motion information predominantly occurs by Castellana, 70/e‑31100 Trevise, Italy) with constant two major parallel pathways to the , where visual luminance of 120 cd/m2 for VA examination using its signals are reintegrated in the visual cortex. Retinal cells Snellen E‑chart with 5 letters on each line to include in the parvocellular pathway are responsible for fine the effect of the crowding phenomenon. In addition, and chromatic stimuli, while cells of the magnocellular Ishihara color test on the Yang vision tester was used pathway are responsible for moving and achromatic for CVD screening. stimuli.[22] Some studies have revealed that monocular The examination was performed at 2 meters distance visual deprivation affects the size of parvocellular and in day . The Ishihara test consists of 16 plates and magnocellular cells in the LGB which is more significant we asked children to read the colored number at the with long‑term involvement of the eye,[22,23] and may middle of each plate monocularly. If the child was able to affect color vision. The color spectrum is perceived by read 13 plates or more correctly, the child was considered different color wavelength sensitive cones which also as normal color vision, otherwise she/he was considered have an effect on control of and refractive to be color vision deficient. The order of presentation of error (RE),[24] therefore problems with color perception the plates was changed from one eye to the other eye to may impact accommodation and refractive errors. prevent cheating. In the present study, we aimed to determine the If the child had , VA and color vision were prevalence of CVD and its correlation with amblyopia assessed with his/her own correction. The eye was and refractive errors among primary school children in suspected to be amblyopic if VA was 20/40 or less, then Tehran, Iran. the measurement was repeated by a 2 mm pinhole and amblyopia was confirmed if VA did not improve to better METHODS than 20/40 with the pinhole. VA was classified according to pinhole VA into 20/20‑20/30, 20/40‑20/100, and less In this population‑based cross‑sectional study, out of a total than 20/100. of 1781 primary schools in Tehran, 36 schools (including an equal number of public and private schools) were selected by random cluster sampling from different Refractive Errors regions (North, South, West, East and Center) of Tehran, The refractive status of all children was measured using the capital city of Iran, from October 2013 to January a photorefractometer (PlusoptiX SO4 GmbH, Nürnberg, 2014. There are six elementary levels in primary schools Germany) with no by a trained technician; in Iran and in all selected schools, 10 students from each this device has a reported sensitivity of 63%‑94% and elementary grade were randomly selected for this study. specificity of 62%‑99%.[25] Photorefraction was repeated The children were aged from 7 to 12 and the number of three times for each subject and the average result was male and female subjects was equal. used for statistical analysis. The measurement range of the A total of 2160 children were selected from 36 photorefraction device is from −7.00 diopter (D) of primary schools. These included 60 students from each to +5.00 D of hyperopia, therefore cases with refractive

Journal of Ophthalmic and Vision Research 2015; Vol. 10, No. 2 131 Color Vision Deficiency and Amblyopia;Rajavi et al errors out of this range were considered to have “high” deviation, median, range, frequency and percentage refractive errors. Anisometropia was defined as spherical data. To evaluate the association of different factors with equivalent (SE) difference of at least one diopter between CVD, we used logistic regression analysis and odds ratio the fellow . Myopia, hyperopia and were with 95% confidence intervals. The multilevel method considered as SE ≤−0.50 D, SE ≥+2.00 D and cylindrical was used to consider the intra‑cluster correlation of power of 0.75 D or more, respectively. observations. All statistical analyses were performed by SPSS software (version 21.0, IBM Co., Chicago, IL, USA). Ocular Deviation P values less than 0.05 were considered as statistically Ocular deviation was checked using the alternate cover significant. test if VA was more than 20/200 and the Krimsky method in subjects with VA less than 20/200. The deviation was RESULTS measured for near (33 cm) and far (6 m). In order to reveal any extraocular muscle dysfunction, the extraocular A total of 2150 children aged 7‑12 (mean, 9.4 ± 1.7) muscles were evaluated in nine different gazes. years were studied. Details of baseline demographics and ocular findings are presented in Table 1. CVD Ocular Structure was detected in 48 children indicating a prevalence of 2.2% (95% CI: 1.5% to 3%). The prevalence of CVD in We assessed the ocular media by examining the red male subjects was significantly higher as compared to ® reflex using a direct ophthalmoscope (HEINE BETA female students [3.5 vs. 1.0%, P < 0.001, Table 1]. 200; Herrsching, Germany). If the size of central Mean and median pinhole VA were lower in children opacity was more than 3 mm, the child was suspected of with CVD as compared to subjects with normal color having . The macula and head were vision [P = 0.035, Figure 1]. There was a significant examined by direct ophthalmoscopy to exclude children difference between children with CVD and normal color with retinal lesions. vision subjects in terms of amblyopia; the prevalence of which was 8.3% (CI: 0.2‑16.4%) in children with Statistical Analysis CVD versus 2.1% (CI: 1.5‑2.08%) in those without To present data, we used mean values, standard CVD [P = 0.005, Tables 1 and 2]. However, there was

Table 1. Demographic and ocular characteristics of children with normal and deficient color vision Factors Total Color vision deficiency OR 95% CI of OR P* No Yes Lower Upper Age (year) Mean±SD 9.4±1.7 9.4±1.8 9.4±1.6 0.99 0.89 1.13 0.986 Median (range) 9 (6-14) 9 (6-13) 9 (7-14) Sex (%) Male 1061 (49.3) 1024 (48.7) 37 (77.1) 3.86 2.28 6.52 <0.001 Female 1089 (50.7) 1078 (51.3) 11 (22.9) 1 Visual acuity Mean±SD 0.17±0.13 0.17±0.12 0.31±0.29 1.43† 1.07 1.91 0.035 Median (range) 0.1 (0.1-1) 0.1 (0.1-1) 0.18 (0.1-0.9) Amblyopia (%) Yes 49 (2.3) 45 (2.1) 4 (8.3) 4.14 1.53 11.21 0.005 No 2101 (97.7) 2057 (97.9) 44 (91.7) 1 Refractive error (%) Yes 1104 (25.9) 1074 (25.8) 30 (31.9) 1.02 0.99 1.05 0.185 No 3155 (74.1) 3091 (74.2) 64 (68.1) 1 Anisometropia (SE difference ≥1.00 D) (%) Yes 85 (4.0) 82 (3.9) 3 (4.3) 1.05 0.26 4.22 0.942 No 2042 (96.0) 1998 (96.0) 44 (95.7) 1 Strabismus (%) Yes 49 (2.3) 46 (2.2) 3 (6.3) 3.01 0.81 11.27 0.101 No 2101 (97.7) 4178 (99.4) 94 (97.9) 1 *Based on multilevel analysis; †Calculated for each line of decreased visual acuity. SD, standard deviation; OR, odds ratio; CI, confidence interval; SE, spherical equivalent; diff, difference; D, diopter; P, probability

132 Journal of Ophthalmic and Vision Research 2015; Vol. 10, No. 2 Color Vision Deficiency and Amblyopia;Rajavi et al

Figure 1. Mean visual acuity (LogMAR) in children with and Figure 2. The percent of color vision deficiency in different without color vision deficiency. VA, visual acuity; logMAR, categories of visual acuity. VA, visual acuity logarithm of the minimum angle of resolution 6.3% had , 8.3% had amblyopia and 4 subjects showed coexisting CVD and amblyopia. The deficiency in color perception occurred in children with VA of 0.3 LogMAR or less. The majority of children were high hyperopic (spherical equivalent ≥+4.00 D) and astigmatic (>1.00 D), half of the cases were exotropic and one had anisometropia [Table 2]. Clinical data of the 49 amblyopic children are presented in Table 3. A comparable proportion of male (51.02%) and female (48.97%) children were amblyopic. There were more cases with high refractive errors among amblyopic children and most strabismic amblyopic children had (8 out of 13 cases, 61.54%). The total sum in some columns in Tables 2 and 3 are not equal to actual numbers of studied students, as photorefraction was not possible in certain children with high refractive errors due to the limited range of the device (−7.00 to +5.00 D), pupillary abnormalities, media opacities or strabismus. Table 4 compares basic characteristics among Figure 3. Comperhensive view of the examined population amblyopic children, those with CVD, and subjects with based on amblyopia and color vision deficiency. CVD, color coexisting amblyopia and CVD, versus normal (no CVD vision deficiency. and no amblyopia) children. Although mean VA among children with no CVD and no amblyopia was lower than no significant correlation between CVD and refractive color vision deficient children, the standard deviation errors, anisometropia, or strabismus [Table 1]. was wider among children with CVD and there was no The prevalence of CVD among different VA categories statistically significant difference. Mean age of amblyopic is presented in Figure 2. The increased positive line children were significantly lower than normal (no CVD slope indicates more reduction of VA; however this and no amblyopia) children (P = 0.033). association should be considered with caution due to small sample size (3 children with CVD among 5 children DISCUSSION with significant reduction of VA). Figure 3 presents a comprehensive view of the normal (no amblyopia and In the current study, in order to improve diagnostic no CVD) examined children and those with amblyopia, accuracy, the Yang vision tester and PlusoptiX SO4 CVD or combination thereof in the studied population. photorefractometer were applied. The former test can Out of 48 children with CVD, 77.1% were male, 16.6% be calibrated for desired distances ranging from 30 cm had hyperopia >+2.00 D, 25% had astigmatism >0.75 D, to 9 m and testing conditions are adjusted automatically;

Journal of Ophthalmic and Vision Research 2015; Vol. 10, No. 2 133 Color Vision Deficiency and Amblyopia;Rajavi et al

Table 2. Basic characteristics of 48 children with color vision deficiency Number Age Sex VA Amblyopia Refraction (D) Anisometropia Strabismus Mixed† (year) (%) (LogMAR) (SE difference OD OS OD OS ≥ 1.00 D) Sphere Cylinder Axis Sphere Cylinder Axis 1 8.0 Girl 0.9 0.9 Yes 4.25 −2.75 180 4.00 −2.00 1 No XT No 2 8.0 Boy 0.4 0.3 Yes 4.50 −1.75 8 H.H* - - Yes No No 3 9.0 Boy 0.3 0.2 Yes 4.25 −3.25 8 3.75 −3.00 179 No No No 4 9.0 Girl 0.1 0.1 No 1.00 −0.50 9 0.50 −0.25 7 No No No 5 11.0 Boy 0.1 0.1 No 1.50 −0.50 15 2.00 −0.25 10 No No No 6 11.0 Boy 0.0 0.1 No 0.00 −0.25 165 −0.75 −0.25 39 No No No 7 9.0 Girl 0.4 0.0 Yes 0.00 −1.00 0 0.00 −3.75 0 No XT No 8 12.0 Boy 0.1 0.0 No 0.25 −0.50 94 −0.25 0.00 0 No No No 9 8.0 Boy 0.0 0.0 No 0.50 0.00 0 1.00 0.00 0 No No No 10 10.0 Girl 0.0 0.0 No 2.50 −0.25 123 2.75 −0.25 35 No No No 11 10.0 Boy 0.0 0.0 No 1.00 −0.25 18 1.25 0.00 0 No No No 12 8.0 Boy 0.0 0.0 No 0.75 −0.50 178 1.75 −0.50 1 Yes No No 13 10.0 Boy 0.0 0.0 No 1.50 −0.75 84 1.25 −0.75 94 No No No 14 14.0 Boy 0.0 0.0 No 0.50 −0.75 178 1.00 −1.25 176 No No No 15 7.0 Boy 0.0 0.0 No 0.50 −0.25 65 0.75 0.00 0 No No No 16 10.0 Boy 0.0 0.0 No 0.50 −0.50 10 0.75 −0.50 7 No No No 17 11.0 Girl 0.0 0.0 No 1.75 −0.75 13 2.25 −1.00 17 No No No 18 10.0 Boy 0.0 0.0 No 1.00 −0.50 87 1.00 −0.25 100 No No No 19 12.0 Boy 0.0 0.0 No 0.25 −0.50 115 0.50 −0.50 54 No No No 20 8.0 Boy 0.0 0.0 No 1.00 −0.25 20 0.75 −0.25 169 No No No 21 10.0 Boy 0.0 0.0 No −1.25 −2.00 175 −0.75 −2.75 2 No No No 22 12.0 Girl 0.0 0.0 No 4.50 −1.50 2 4.75 −0.75 165 No No No 23 7.0 Boy 0.0 0.0 No 1.00 −0.50 135 1.25 −0.50 73 No No No 24 9.0 Boy 0.0 0.0 No 1.00 −0.50 93 0.75 −0.25 53 No No No 25 8.0 Boy 0.0 0.0 No 0.25 −0.50 92 0.50 −0.25 95 No No No 26 9.0 Boy 0.0 0.0 No 1.25 −0.50 178 1.25 0.00 0 No No No 27 8.0 Boy 0.0 0.0 No 0.00 −0.25 53 −0.25 −1.25 177 No No No 28 9.0 Boy 0.0 0.0 No 1.75 −1.25 26 1.25 −0.75 7 No No No 29 11.0 Boy 0.0 0.0 No 0.50 −0.25 103 0.50 −0.50 81 No No No 30 12.0 Boy 0.0 0.0 No 0.25 −0.25 128 0.75 0.00 0 No No No 31 9.0 Girl 0.0 0.0 No 1.00 −0.25 175 0.75 −0.50 3 No No No 32 9.0 Boy 0.0 0.0 No 1.50 −0.50 82 1.00 −0.50 133 No No No 33 7.0 Boy 0.0 0.0 No 1.50 −0.50 131 0.75 −0.25 71 No No No 34 8.0 Boy 0.0 0.0 No 1.75 −0.75 107 1.00 −0.25 69 No No No 35 9.0 Girl 0.0 0.0 No 0.50 −0.25 116 0.50 −0.25 65 No No No 36 10.0 Girl 0.0 0.0 No 1.00 −1.00 10 1.25 −1.25 173 No No No 37 11.0 Girl 0.0 0.0 No 0.25 −0.25 108 0.50 −0.50 43 No No No 38 8.0 Boy 0.0 0.0 No 1.25 −0.75 87 1.00 −0.50 115 No No No 39 10.0 Boy 0.0 0.0 No 0.25 −0.25 169 0.25 0.00 0 No No No 40 9.0 Boy 0.0 0.0 No 1.75 −0.50 1 1.25 −0.25 25 No No No 41 10.0 Boy 0.0 0.0 No 0.50 0.00 0 0.50 0.00 0 No No No 42 9.0 Girl 0.0 0.0 No - - - 1.25 −1.00 179 - No No 43 12.0 Boy 0.0 0.0 No 0.00 −0.50 116 0.75 −0.25 30 No No No 44 9.0 Boy 0.0 0.0 No 1.00 −0.50 165 1.00 −0.75 20 No No No 45 9.0 Boy 0.0 0.0 No 1.00 −0.25 105 0.75 −0.25 7 No No No 46 7.0 Boy 0.0 0.0 No 1.50 −0.25 148 2.50 −0.25 70 Yes No No 47 8.0 Boy 0.0 0.0 No 0.50 −0.25 38 0.50 −0.25 160 No XT No 48 9.0 Boy 0.0 0.0 No 0.00 −0.25 64 0.00 0.00 0 No No No Mean 9.4 Male: 0.05 0.04 8.3% 1.08 −0.63 - 1.04 −0.60 - 6.25% 6.3% 0% 77.08% SD 1.6 0.16 0.14 1.20 0.65 1.08 0.79 *H.H, high hyperopia which was out of range of photorefractometer; †Mixed, Combination of anisometropia and strabismus. VA, visual acuity; OD, oculus dexter; OS, oculus sinister; LogMAR, logarithm of the minimum angle of resolution; SE, spherical equivalent; diff, difference; M, male; SD, standard deviation; D, diopter; No, number; y, year

134 Journal of Ophthalmic and Vision Research 2015; Vol. 10, No. 2 Color Vision Deficiency and Amblyopia;Rajavi et al

Table 3. Basic characteristics of 49 amblyopic children Number Age Sex VA CVD Refraction (D) Anisometropia Strabismus Mixed† (year) (LogMAR) (SE difference OD OS OD OS ≥1.00 D) Sphere Cylinder Axis Sphere Cylinder Axis 1 7.0 Boy 0.5 0.6 No 0.00 −3.00 0 0.00 −2.75 0 No ET No 2 11.0 Girl 0.0 0.3 No 1.75 −1.25 179 1.75 −0.75 13 No No No 3 9.0 Girl 0.3 0.2 No −2.75 −0.25 97 −2.75 −0.50 70 No XT No 4 11.0 Girl 0.3 0.0 No 2.00 0.00 0 3.50 −0.50 125 Yes No No 5 12.0 Girl 0.3 0.3 No −0.25 −0.75 95 0.00 −0.75 82 No No No 6 11.0 Boy 0.7 0.7 No ------No No 7 8.0 Boy 0.3 0.0 No 2.75 −3.50 12 0.75 −0.75 171 No No No 8 9.0 Boy 0.3 0.2 Yes 4.25 −3.25 8 3.75 −3.00 179 No No No 9 7.0 Girl 0.1 0.3 No 2.25 −0.75 169 0.00 −4.00 0 No No No 10 7.0 Girl 0.3 0.3 No 1.25 −3.50 9 0.50 −2.75 178 No No No 11 8.0 Girl 0.2 0.3 No 2.50 −2.25 7 3.50 −3.00 179 No ET No 12 11.0 Boy 0.3 0.2 No ------No No 13 10.0 Girl 0.3 0.0 No 0.00 −2.25 0 0.00 −2.00 0 No ET No 14 8.0 Boy 0.3 0.0 No 1.50 −0.25 105 0.75 0.00 0 No ET No 15 7.0 Girl 0.2 0.4 No 2.00 −0.50 158 3.00 −0.50 6 Yes No No 16 7.0 Girl 0.3 0.0 No 3.75 −2.25 5 1.25 −0.75 169 Yes No No 17 9.0 Girl 0.3 0.2 No 1.00 −2.75 7 0.75 −1.50 174 No No No 18 7.0 Girl 0.4 0.4 No 0.00 −4.25 0 0.00 −3.00 0 No No No 19 12.0 Girl 0.0 1.0 No −0.25 −0.50 77 4.75 −2.00 128 Yes XT Yes 20 8.0 Boy 0.3 0.0 No ------No No 21 12.0 Boy 0.3 0.2 No 0.25 −1.00 178 0.25 −0.50 9 No ET No 22 7.0 Girl 0.3 0.1 No 3.75 −3.75 0 0.00 −3.50 0 No XT No 23 7.0 Girl 0.5 0.7 No −3.25 −2.75 175 0.00 −4.00 0 Yes No No 24 9.0 Girl 0.4 0.0 Yes 0.00 −1.00 0 0.00 −3.75 0 No XT No 25 9.0 Girl 0.6 0.0 No 3.00 −0.50 175 2.75 −1.50 167 No No No 26 8.0 Girl 0.9 0.9 Yes 4.25 −2.75 180 4.00 −2.00 1 No XT No 27 9.0 Girl 0.3 0.3 No 0.50 −5.00 2 0.25 −5.00 2 No No No 28 12.0 Boy 0.1 0.3 No 0.75 −0.50 77 1.75 −1.50 153 No No No 29 12.0 Girl 0.0 0.5 No 0.25 −0.25 118 0.75 −0.25 40 No ET No 30 8.0 Boy 0.0 0.3 No 1.00 0.00 0 - - - - No No 31 9.0 Boy 0.3 0.3 No 4.25 −2.75 8 3.00 −2.50 175 Yes No No 32 7.0 Girl 0.2 0.3 No 0.25 −4.75 2 0.25 −4.50 171 No No No 33 7.0 Boy 0.3 0.1 No 1.75 −3.75 7 1.50 −3.25 165 No No No 34 8.0 Boy 0.4 0.3 Yes 4.50 −1.75 8 H.H* - - Yes No No 35 9.0 Boy 0.3 0.1 No 0.00 −0.50 0 0.00 −0.50 0 No No No 36 10.0 Boy 0.3 0.2 No −2.00 −0.25 177 −2.50 −0.50 9 No No No 37 8.0 Girl 0.4 0.5 No 5.00 −3.25 2 3.25 −2.75 179 Yes No No 38 7.0 Boy 0.3 0.3 No 1.75 −2.75 10 2.00 −2.50 173 No No No 39 8.0 Boy 0.2 1.0 No ------No No 40 8.0 Girl 0.3 0.3 No ------No No 41 12.0 Girl 0.9 0.0 No 0.25 −0.25 108 0.25 −0.25 63 No ET No 42 8.0 Boy 0.3 0.1 No 1.00 −4.75 3 0.75 −2.25 176 Yes No No 43 10.0 Boy 0.3 0.1 No 4.50 −1.00 1 2.75 −1.75 1 Yes ET Yes 44 7.0 Boy 0.3 0.3 No 3.25 −2.00 179 4.25 −2.25 78 No No No 45 8.0 Boy 0.0 0.3 No 1.50 −0.50 18 3.50 −0.75 154 Yes No No 46 12.0 Boy 0.4 0.0 No 0.50 −4.25 10 0.50 −0.50 2 Yes No No 47 7.0 Boy 0.3 0.3 No 2.00 −1.25 179 3.50 −1.50 3 Yes No No 48 11.0 Boy 0.3 0.2 No 3.50 −3.25 13 3.25 −4.25 74 No No No Mean 8.0 Boy 0.3 0.3 No 2.00 −1.25 179 3.50 −1.50 3 Yes No No SD 8.9 Male: 0.31 0.28 8.2% 1.35 −1.78 - 1.24 −1.67 - 28.6% 26.5% 4.1% 51.02% 1.8 0.19 0.25 1.86 1.55 1.72 1.43 *H.H: high hyperopia which was out of range of photorefractometer; †Mixed: Combination of anisometropia and strabismus. VA, visual acuity; OD, right eye; OS, left eye; LogMAR, logarithm of minimum angle of resolution; CVD, color vision deficiency; SE, spherical equivalent; diff, difference; M, male; F, female; SD, standard deviation; D, diopter; No, number; y, year

Journal of Ophthalmic and Vision Research 2015; Vol. 10, No. 2 135 Color Vision Deficiency and Amblyopia;Rajavi et al

thus, accurate color vision testing is possible at different ** ‡ distances. Its luminance can also be set from 80 to (%)

0 (0) 0 (0) 2 0.031 0.001 0.031 0.001

2 (4.4) 6 (0.3) 320 candela (cd)/m and the commonly used value Mixed is 120 cd/m2 which is constant for all measurements.

‡ Therefore, we tested color perception in all children under standard conditions of our system with more

(%) stability as compared with the conventional Ishihara test. 0.001 0.801 0.053 2 (50) 1 (2.3) <0.001 35 (1.7) 11 (24.4) The Ishihara test was also applied in our study as it Strabismus is commonly used to screen for red‑green CVD and can

‡ be learned easily and performed rapidly in children. It contains of ten characters differing in size (thinnest portions being under 0.5 cm), parallel to VA results.[26] 0.705 1 (25) <0.001 <0.001 <0.001

3 (6.25) 70 (3.4) We performed photorefraction with no cycloplegia 14 (28.6) according to manufacturer recommendations, since ≥1.00 D) (%) (SE difference Anisometropia induced peripheral aberrations due to a dilated makes measurement of astigmatism more difficult and there is a possibility of off‑axis refraction. In addition, - - - - photorefraction was performed at a longer working −2.9±0.9 Cylinder −0.6±0.79 −1.67±1.43 −0.52±0.59 distance (1 m or more) as compared to other refractive

OS error measurement tools such as a retinoscope or Based on analysis of variance: adjusted for multiple comparison by §

† autorefractometer, therefore accommodation might be - - - - more relaxed. 3.9±0.2 Sphere 1.04±1.08 1.24±1.72 0.83±0.79 In our study, 48 out of 2150 children had CVD [Table 1]. The male to female ratio was 3.5 with higher prevalence Based on GEE analysis, adjusted for multiple comparison by Bonf erroni method. § in male subjects which is consistent with other [5,12] Refraction (D) studies. CVD is usually inherited by an X‑linked 0.999 0.997 >0.99 >0.99

−2.2±1 [5]

Cylinder recessive pattern and studies on European Caucasians −0.63±0.65 −1.78±1.55 −0.49±0.58

OD have revealed that CVD is approximately 20 times more prevalent among male as compared to female subjects.[1‑5] The difference in male to female ratio in our population, 0.999 0.998 0.999 0.999 4.3±0.1 Sphere 1.08±1.2

1.35±1.86 0.83±0.82 as compared to European studies, may be the lower age or a different genetic basis for CVD in our population. We observed that all four patients with combined - - - -

OS CVD and amblyopia had a VA of 20/40 or less [Table 2]

0.5±0.4 [27] § 0.04±0.14 0.28±0.25 0.12±0.04 which is comparable to the study by Bradley et al

VA reporting that all patients with combined CVD and amblyopia had VA of less than 20/50. We also found a

OD statistically significant correlation between CVD and 0.579 0.006 <0.001 <0.001 0.5±0.3

0.05±0.16 0.31±0.19 0.12±0.04 VA which means CVD was more prevalent in children with lower VA [Figures 1 and 2] as von Noorden[28] and other researchers have stated.[20,27,29] These findings are consistent with studies showing that color perception [2] male/

‡ is affected when VA decreases to less than 20/50. 0.003 0.745 0.957 <0.001 2/2 (50) Furthermore, it has been reported that color vision Sex 35/9 (79.5) 23/22 (51.1) loss occurs more frequently when the VA is less than 1001/1056 (48.7) female (male %) 20/400[20] or 20/200.[29]

[26] † McCulley et al reported that the Ishihara test was the color test most dependent on good VA and it Age 0.993 0.993 0.033 0.992 (year) 9.4±1.6 8.9±1.8 8.5±0.6 9.5±1.7 was not affected up to VA of 0.72 LogMAR (20/106). Based on logistic regression: adjusted for multiple comparison by Bonferroni method, ‡ In our study, 6 of 8 eyes (75%) with VA worse than 0.7 LogMAR did not show CVD which is not consistent with this assumption. It seems that determination of VA as an accuracy criterion for the Ishihara test should be considered with caution [Table 2]. Although there was no difference between normal and *Both: Combination of color vision deficiency and amblyopia, **M ixed: anisometropia strabismus, Bonferroni method, VA, visual acuity; LogMAR, logarithm of minimum angle resolu tion; OD, right eye; OS, left SE, spherical equivalent; di ff, difference; CVD, color vision deficiency; M, male; F, female ; D, diopter; y, year; PNC, correlation between normal (No CVD & No amblyopia) and children; PNA, children amblyopic children; PNB, correlation between normal (No CVD & No amblyopi a) children and those with coexisting of both; PCA, amblyopic Table 4. Comparison of all the basic characteristics among examined children CVD Amblyopia Both** Normal (no CVD amblyopia) no and PCA PNC PNA PNB color vision deficient children considering strabismus

136 Journal of Ophthalmic and Vision Research 2015; Vol. 10, No. 2 Color Vision Deficiency and Amblyopia;Rajavi et al and refractive errors, amblyopia was significantly more REFERENCES common among children with CVD [P = 0.005, Table 1]. Qian et al[30] found a lower incidence of myopia among 1. Waaler GH. Über die Erblichkeitsverhältnisse der verschiedenen Arten von angeborener Rotgrünblindheit. Acta Ophthalmol children with abnormal color perception as compared to 1927;5:309‑345. normal (no CVD and no amblyopia) children while in the 2. Feig K, Ropers HH. On the incidence of unilateral and present study, there was no difference between normal bilateral colour blindness in heterozygous females. Hum Genet color vision and CVD children in terms of myopia. 1978;41:313‑323. Ocular deviation especially exotropia was seen in 3. Kherumian R, Pickford RW. Hérédité et fréquence des Anomalies Congénitales du Sens Chromatique: (dyschromatopsies). Paris: 50% of children with coexisting amblyopia and CVD Vigot Frères. 1959. p. 63‑67. whereas 25% of them showed anisometropia [Table 2]. 4. Crone RA. Incidence of known and unknown colour vision Bradley et al[27] also observed strabismus in 66% of defects. A study of 6526 secondary school in Amsterdam. children with coexisting amblyopia and CVD with Ophthalmologica 1968;155:37‑55. no difference among certain deviation types but the 5. Birch J. Worldwide prevalence of red‑green color deficiency.J Opt majority had unsteady foveal or eccentric fixation. Soc Am A Opt Image Sci Vis 2012;29:313‑320. [19] 6. Sato S. Statistical observations on congenital abnormalities in Koçak‑Altintas et al found no relationship between colour vision in Japan. Acta Soc Ophthalmol Jpn 1935;38:2227‑2230. CVD and any types of amblyopia such as anisometropia 7. Chan E, Mao WS. Colour‑blindness among the Chinese. Br J or strabismus which is comparable to our results. Ophthalmol 1950;34:744‑745. Bradley et al[27] reported that most amblyopic children 8. Yang C, Chiang JC, Feng PH, Yang NH. Color‑blindness among with CVD were hyperopic (sphere ≥+2.50 D). In the present the Chinese. Chin Med J 1958;76:283‑284. study, 4 children had both amblyopia and CVD, and 5 out of 9. Iinuma I, Handa Y. A consideration of the racial incidence of congenital dyschromats in males and females. Mod Probl 6 amblyopic eyes had hyperopia more than + 4.00 D which Ophthalmol 1976;17:151‑157. is comparable to Bradley’s findings [Table 2]. 10. Kilborn LG, Beh YT. The incidence of color‑blindness among the One of the limitations of the current study is that Chinese. Science 1934;79:34. examined children were screened only for red‑green CVD 11. Kim HB, Lee SY, Choe JK, Lee JH, Ahn BH. The incidence of since the Ishihara test is not able to detect blue‑yellow congenital color deficiency among Koreans. J Korean Med Sci 1989;4:117‑120. deficiency. Children who were diagnosed with CVD were 12. Alabdelmoneam M. Prevalence of congenital color vision defects not retested using another color vision test with more in Saudi females of Arab origin. 2011;82:543‑548. sensitivity to validate our observations. Moreover, lack of 13. Harrad R, Sengpiel F, Blakemore C. Physiology of cycloplegic refraction and determination of best corrected in strabismic amblyopia. Br J Ophthalmol 1996;80:373‑377. VA among all children was another limitation of our study. 14. Williams C, Papakostopoulos D. Electro‑oculographic In summary, although CVD was correlated with abnormalities in amblyopia. Br J Ophthalmol 1995;79:218‑224. amblyopia and decreased vision, there was no 15. Holmes JM, Clarke MP. Amblyopia. Lancet 2006;367:1343‑1351. 16. von Noorden GK, Crawford ML. The lateral geniculate nucleus relationship between CVD and the type of amblyopia, in human strabismic amblyopia. Invest Ophthalmol Vis Sci refractive error, anisometropia and ocular deviation. 1992;33:2729‑2732. Exotropia and hyperopia were the most common form 17. Kiorpes L, McKee SP. Neural mechanisms underlying amblyopia. of ocular deviation and refractive error among children Curr Opin Neurobiol 1999;9:480‑486. with coexisting CVD and amblyopia. 18. Davis AR, Sloper JJ, Neveu MM, Hogg CR, Morgan MJ, Holder GE. Electrophysiological and psychophysical differences between early‑ and late‑onset strabismic amblyopia. Invest Acknowledgments Ophthalmol Vis Sci 2003;44:610‑617. This study was supported by the Ophthalmic Research 19. Koçak‑Altintas AG, Satana B, Koçak I, Duman S. Visual acuity and color vision deficiency in amblyopia.Eur J Ophthalmol 2000;10:77‑81. Center, Shahid Beheshti University of Medical Sciences 20. Almog Y, Nemet A. The correlation between visual acuity and and Basir Eye Safety Research Center. color vision as an indicator of the cause of visual loss. Am J The authors would like to thank all the children Ophthalmol 2010;149:1000‑1004. and their families who participated in this study, as 21. Komatsu H. Mechanisms of central color vision. Curr Opin well as Shadi Akbarian, Masoumeh Kalantarion, Simin Neurobiol 1998;8:503‑508. Kalantarion, Bahar Kheiri, Shirin Mohebi and Bahar 22. Davis AR, Sloper JJ, Neveu MM, Hogg CR, Morgan MJ, Holder GE. Differential changes in color and motion‑onset Safdari for their efforts in coordinating the fieldwork visual evoked potentials from both eyes in early‑ and and their assistance in data collection. late‑onset strabismic amblyopia. Invest Ophthalmol Vis Sci 2008;49:4418‑4426. Financial Support and Sponsorship 23. Lunghi C, Burr DC, Morrone MC. Long‑term effects of revealed with binocular rivalry gratings modulated Nil. in luminance and in color. J Vis 2013;13:1-15. 24. Rucker FJ, Kruger PB. Cone contributions to signals for accommodation and the relationship to refractive error. Vision Conflicts of Interest Res 2006;46:3079‑89. There are no conflicts of interest. 25. Schimitzek T, Haase W. Efficiency of a video‑autorefractometer

Journal of Ophthalmic and Vision Research 2015; Vol. 10, No. 2 137 Color Vision Deficiency and Amblyopia;Rajavi et al

used as a screening device for amblyogenic factors. Graefes Arch 28. von Noorden GK. and Ocular Motility: Clin Exp Ophthalmol 2002;240:710‑716. Examination of Patient‑III Sensory Signs Symptoms and 26. McCulley TJ, Golnik KC, Lam BL, Feuer WJ. The effect of Adaptation in Strabismus. St. Louis: Mosby Co.; 1990. p. 219‑231. decreased visual acuity on clinical color vision testing. Am J 29. François J, Verriest G. Color discrimination in strabismic Ophthalmol 2006;141:194‑196. amblyopia. Doc Ophthalmol 1967;23:318‑331. 27. Bradley A, Dahlman C, Switkes E, De Valois K. A comparison 30. Qian YS, Chu RY, He JC, Sun XH, Zhou XT, Zhao NQ, et al. Incidence of color and luminance discrimination in amblyopia. Invest of myopia in high school students with and without red‑green color Ophthalmol Vis Sci 1986;27:1404‑1409. vision deficiency.Invest Ophthalmol Vis Sci 2009;50:1598‑1605.

138 Journal of Ophthalmic and Vision Research 2015; Vol. 10, No. 2