Abstract
Purpose
To investigate how refractive imbalance affects binocular vision parameters, reading performance, and vision-related reading difficulty symptomatology after short periods of reading with different simulated ophthalmic lens power conditions in expert adult readers.
Methods
Eighteen adult participants (18–35 years of age) were recruited. They were expert readers, defined as currently studying, or previously studied to, at least a bachelor's degree tertiary education level. Refractive imbalance conditions were simulated by placing −2.00, −1.00, 0.00, +1.00, and +2.00 diopters (D) ophthalmic lenses in front of the dominant eye over their full refractive error correction. For each condition, participants were required to read sets of three paragraphs from the background section of an academic journal paper, after which reading comprehension, reading speed, symptomatology, visual acuity, and binocular vision status were assessed for each set through refractive imbalance conditions.
Results
A significant reduction of binocular visual acuity was observed for distance (+2.00 D condition) and near (±2.00 D conditions) viewing distances. The greater the refractive imbalance stimulus provided to the dominant eye monocularly, the more underfocused the binocular accommodative response. Simulated refractive imbalance did not affect reading speed and comprehension. Stereoacuity and subjective vision-related reading difficulty symptoms worsened with increased absolute refractive imbalance.
Conclusions
Simulated refractive imbalance did not affect reading performance for the short reading task but resulted in statistically significant reductions in clarity, increased binocular difficulties, and visual discomfort. During reading, full correction of refractive imbalance is beneficial and recommended.
Keywords: refractive imbalance, reading performance, binocular vision, vision-related reading symptom, visual acuity
Uncorrected refractive error (URE), the leading cause of vision impairment in the world,1 is often correctable with spectacles, contact lenses, and refractive surgery. However, among people with URE worldwide, the unmet need for refractive correction coverage has been estimated as 64%.2 Of people with URE, 12.3% to 15.9% have asymmetric URE between the two eyes,3–6 which may be termed anisometropia (refractive imbalance), defined as a difference of at least 1.00 diopter (D) in spherical equivalent refraction between the two eyes. Hence, there are large numbers of people with URE and unbalanced refractive error who do not wear spectacles. Among young people, reasons for not wearing spectacles when owning them include “did not feel the need,” disapproval or teasing from family or peers, low affordability, dislike of aesthetic appearance, discomfort (heavy, poorly fitting, uncomfortable, glary spectacles), and broken and lost spectacles.7 Among older adults, being unmotivated or experiencing difficulty adapting to spectacles resulted in poor compliance.8
Uncorrected refractive imbalance is associated with abnormality of binocular vision (BV) functions,9,10 including the ability to accurately fuse, accommodate, perceive, and combine information from the two eyes into a single percept. For example, when simulating refractive imbalance by placing a ±1.00 to 3.00 D powered ophthalmic or contact lens over one eye, stereoacuity worsened,9,11,12 and foveal suppression scotomas increased in size with increasing refractive imbalance.13 In patients with habitual (i.e., nonsimulated) refractive imbalance, binocular fusion ability reduces with increasing magnitude of refractive imbalance.10 Such changes may affect binocular summation,14 the advantage of looking with both eyes compared to looking with one eye. Binocular summation has been documented to occur for visual functions, including visual acuity (VA),15 contrast sensitivity, and flicker detection.16 Functionally, binocular vision is associated with faster response times over monocular vision17 and increased efficiency of reading, as indicated through decreased proportion of regressions and decreased fixation duration per text line over monocular vision during reading tasks.18
Reading behaviors are also affected by refractive imbalance. In children, reading speed and comprehension, measured by the Neale Analysis of Reading Ability test,19 were reduced with a −0.75 D simulated refractive imbalance over one eye.20 Children with habitual refractive imbalance had lower reading speeds on average compared with a control group.21 It is unknown how refractive imbalance affects reading speed and comprehension in expert adult readers.
The aim of this study was to investigate how simulated refractive imbalance affects reading performance, BV parameters, and symptomatology after short reading tasks in expert adult readers in a real-life reading task. To address the aim, three specific hypotheses were investigated: simulated refractive imbalance will result in changes in (1) how the visual system uses information from the two eyes (i.e., binocular vision), as indicated by poorer ability to fuse, accommodate, perceive, and combine information from the two eyes; (2) reading performance, as indicated by reading speed and comprehension; and (3) subjective vision-related reading difficulty symptoms.
Methods
Participants
The scope of the study was limited to “expert readers,” defined here as individuals who primarily read at a high level for their occupation (e.g., tertiary studies at the bachelor's degree level or higher), to minimize the impact of education level on the findings. Table 1 presents the inclusion and exclusion criteria of participant recruitment. The exclusion criteria included the following confounding factors: BV problems, habitual refractive imbalance, age-related pathology, and presbyopia.22 In visit 1, the participants were screened according to the inclusion and exclusion criteria, including by conducting binocular and monocular vision assessments.23,24 Written informed consent was obtained from the participants. The study protocol was approved by the Human Research Ethics Committee of University of Canberra, Canberra, Australia, in accordance with the Declaration of Helsinki.
Table 1.
Participant Inclusion and Exclusion Criteria
| Inclusion | Exclusion |
|---|---|
| Aged 18–35 years | Having habitual vision correction of one or both eyes more than 0.50 D from subjective refraction |
| Normal visual health | Having habitual refractive imbalance more than 0.50 D between two eyes |
| Currently studying or previously studied to at least a bachelor's degree tertiary education level in English | History of reading dyslexia |
| Monocular and binocular vision disorder |
Study Design
A repeated-measures study design was used with random ordering of refractive imbalance conditions and random ordering of text sets, by draw of lots methods; the author (TL) picked one piece of paper for the conditions and texts to minimize any systematic effects, including learning or fatigue, on average. The refractive imbalance conditions were simulated using spherical ophthalmic lenses in a trial frame, −2.00 D, −1.00 D, 0.00 D, +1.00 D, and +2.00 D, in front of the sighting dominant eye over their full refractive error correction.25 These powers were selected because prevalence studies commonly use 1.00 D intervals,26,27 and the maximum of ±2.00 D (approximately 4% of magnification difference) was chosen to avoid any undesirable effect of unequal perceived image size between two eyes (i.e., aniseikonia; up to 5% of magnification difference between the eyes is tolerable28), in addition to any blurring effect due to URE.
Each participant completed two visits. In visit 1, participants underwent vision assessment, including measurements of VA, refractive error (noncycloplegic), and BV assessment (see “Outcome Measurements” section for details), and completed the Convergence Insufficiency Symptom Survey (CISS) questionnaire (score of 21 or higher is considered suggestive of convergence insufficiency)29 to determine BV and refractive status, as well as habitual symptomatology. Participants who met the inclusion criteria were then asked to read a given text silently through their full refractive error correction in a trial frame; reading speed was measured, and participants completed the reading comprehension questionnaire immediately after reading the text as baseline data. All participants read the same baseline text. The measurements records in visit 1 were named as baseline data.
In visit 2, participants wore a trial frame with the same full refractive error correction as visit 1, but over their dominant eye, five different spherical powers were added in a randomized order to simulate refractive imbalance. The participants were naive as to which power was used. Participants were given 1 minute of adjustment time with each condition, then read a given text (randomized over participants), followed by VA and clinical BV tests. After these tests, the reading comprehension and vision-related reading difficulty symptomatology questionnaires were completed. Then the simulated lenses were removed, and participants had a 5-minute rest without wearing the trial frame between each refractive imbalance condition.
During the experiment, multiple participants stated that the time delay between the reading task and the comprehension test (due to intervening clinical BV tests) may have affected their performance in the comprehension test. However, the time delay would have been the same for all conditions, hence affecting all conditions equally, and should not have affected the results. Nevertheless, as there could have been a ceiling effect, we recruited a second group of participants who had their comprehension assessed immediately after reading the text. Hence, participants were divided into two groups: those who had comprehension assessed after a 30-minute delay, during which the clinical BV tests were conducted (study 1), and those assessed without delay (study 2). The first nine participants were included as the study 1 group and the other nine participants were in the study 2 group.
Stimuli
The reading texts comprised excerpts of paragraphs from a journal article, rather than existing standardized texts, to maximize their relevance to real life. The journal article selected was titled “Gamified Learning in Higher Education: A Systematic Review of the Literature,”30 because the topic of this article dealt with education, and all tertiary educated participants have experience of up to tertiary education. The selected article also did not have high levels of discipline-specific jargon that would be a hurdle for readers from different disciplinary backgrounds. The logical structure in each text set followed academic conventions by introducing one piece of knowledge per paragraph. The baseline and experimental 1, 2, 3, 4, and 5 reading text sets consisted of three paragraphs each; the number of words was 502, 410, 496, 558, 358, and 303 for each set, respectively. Readability for text sets was matched to be at least college grade level.31,32 A pilot study was conducted that showed no significant difference in reading speed, comprehension score, and vision-related reading difficulty symptomology scores among text sets for a different group of age-matched readers (Supplementary Material S1). The text followed a two-column format, where columns were 8.25 cm wide with 0.8 cm space and Times New Roman font of size 10 (3.5 mm width for A4 size at a 40-cm reading distance).
The reading text was presented on a Dell LED backlit LCD monitor (Dell Technologies, Austin, TX, USA; model: P2319H). The 23-inch monitor had 1,920 × 1,080 resolution at 60 frames per second display. The monitor was set at 94% brightness, 91% contrast, and 100% sharpness to simulate a similar condition to printed paper, which corresponded to a luminance of 40.34 cd/m2 for the black text with white background and 103.03 cd/m2 for the white background. The monitor was placed at 40 cm, considered a standard reading distance,33 in front of the participants. Each reading text set was presented using the program “Acrobat Reader DC” and adjusted to 87% of zoom magnification to match A4-sized paper.
Outcome Measurements
Distance (6 m) and near (40 cm) VA were assessed using logMAR Sloan letter charts (Thomson Software Solutions, Welham Green, UK) and near letter charts (Good-lite, Elgin, IL, USA), respectively. The extent of binocular summation for near VA was calculated using the following formula: Summation = better eye VA − binocular VA; positive values were considered binocular summation and negative values binocular inhibition. Note here that better VA means lower logMAR values.
The clinical BV assessment included near point of convergence and binocular amplitude of accommodation using a Royal Airforce ruler, binocular accommodation facility (±2.00 D flippers), vergence facility (3 Δ base-in/12 Δ base-out prism flippers), stereopsis (random dot test), dissociated distance and near phoria (Von Graefe), distance and near fusional reserve (Risley prisms in a phoropter), monocular and binocular relative accommodation tests at near, and binocular fused cross cylinder test (FCC) and monocular cross cylinder test (MCC) at near. The binocular FCC at near showed how the visual system adapted to the unequal inputs between the two eyes when looking at a chart 40 cm away. The MCC results showed each eye's accommodative state in the presence of stimulation while the other eye was occluded. Values were evaluated as being within or outside ±1 standard deviation from expected mean values24 and considered customarily expected or unexpected, respectively.24
Reading Performance
The participants were instructed as follows: “You will read the given reading set only once, and after reading, you need to answer the 5 given questions based on the content of the reading set.” Time taken to read the text was recorded using a stopwatch with start indication by the instructor (TL) and stop indication by participants, and then reading speed was calculated in words per minute. Total reading time and calculated reading speed for each set are presented in Supplementary Material S2. Reading comprehension for each reading set was assessed using true/false questions with associated confidence, on a 6-point Likert scale, to gain greater insight into thinking processes of the participants. The answers were summed, resulting in total scores ranging from 0 to 25 for the five questions, where higher scores indicated more confidently correct responses, and lower scores indicated more incorrect and low-confidence responses. The questions for reading comprehension were created by the author (TL) and reviewed and revised by other authors (JvB, ML, MYB).
Vision-Related Reading Difficulty Symptomatology
In study 1 (30-minute delay group), the participants were asked to report how they felt while reading, including any adverse symptoms, during the reading tasks. The symptoms reported by participants while reading in study 1 were developed into items of a questionnaire to assess the severity of vision-related reading difficulty symptoms under different refractive imbalance conditions in study 2 (nondelay group). The questionnaire consisted of five items (given in Supplementary Material S3). For items 1, 2, 4, and 5, no negative symptoms were scored as 0, slightly symptomatic as 1, very symptomatic as 2, and completely symptomatic as 3. For item 3, the options were different, with time able to read as follows: a long time of more than 30 minutes to 2 hours was scored as 0, a moderate time of 15 to 30 minutes as 1, a short time of 5 to 10 minutes as 2, and intolerable at 0 minutes as 3.
Statistical Analysis
All data analyses were performed using JAMOVI34 and SPSS (Statistical Package for Social Sciences, version 27.0; SPSS, Inc., Chicago, IL, USA) statistical software. Paired t-tests were used to compare baseline (visit 1) and the 0.00 D refractive imbalance condition after reading (visit 2) in VA and BV parameters; as there were numerous parameters, the statistically significant P value was adjusted to the calculated false discovery rate (FDR) using the Benjamini–Hochberg correction, with the threshold set as FDR-adjusted P < 0.05.35 Separate repeated-measures ANOVA with Huynh–Feldt correction was used with refractive imbalance as the within-subject factor and the following dependent variables: (1) near VA, (2) BV parameters, (3) reading speed, (4) reading comprehension score, and (5) symptomatology score. The between-groups factor was delay (study 1 group) or no delay (study 2 group) of the comprehension assessment (mixed ANOVA). A level of P < 0.05 was considered statistically significant. Linear and nonlinear (quadratic) contrast analyses were used to assess the impact of refractive imbalance on clinical BV parameters. For significant effects, post hoc paired comparison tests with Bonferroni correction were used to identify significant differences between the two conditions.
Results
Eighteen adults (6 men, 12 women) volunteered, and all participants met the criteria. The mean age of participants was 26.77 ± 5.07 years (range, 21–35 years). There was no statistically significant difference in the mean age between the two sexes (t(17) = 1.35, P = 0.20, d = 0.67). The mean CISS score was 16 ± 2.22. The mean refractive error (spherical equivalent) was −1.74 ± 0.47 D for the dominant eye and −1.61 ± 0.50 D for the nondominant eye. The best-corrected visual acuity at near was −0.09 ± 0.01, −0.09 ± 0.01, and −0.12 ± 0.02 logMAR in the dominant eye, nondominant eye, and binocularly, respectively.
There were no significant differences in binocular and monocular VA between baseline and the 0.00 D refractive imbalance condition after reading (FDR-adjusted P > 0.05). Across simulated refractive imbalance conditions, both distance and near VA in the dominant eye showed significant differences (distance: F(1.6, 26.7) = 47.9, P < 0.001, η2p = 0.74; near: F(4, 68) = 11.5, P < 0.001, η2p = 0.40). Post hoc paired comparison testing showed that at distance, VA was poorer with refractive imbalance with plus ophthalmic lenses (0.08 ± 0.04 and 0.46 ± 0.05 logMAR in +1.00 D and +2.00 D, respectively) than the 0.00 D (−0.11 ± 0.02 logMAR) condition (t(17) = 5.26, P < 0.001, d = 1.24 between +1.00 D and t(17) = 11.05, P < 0.001, d = 2.60 between +2.00 D). However, at near, refractive imbalance with minus ophthalmic lenses (−0.03 ± 0.02 and −0.05 ± 0.01 logMAR in −2.00 D and −1.00 D, respectively) were associated with poorer VA than 0.00 D (−0.10 ± 0.02 logMAR) (t(17) = 3.12, P = 0.006, d = 0.74 between −1.00 D and t(17) = 4.54, P < 0.001, d = 1.07 between −2.00 D).
Binocular VA results after reading for a short period with simulated refractive imbalance are presented in Figure 1. The binocular VA results showed significant differences across simulated refractive imbalance conditions at all distances (F(3.9, 66.9) = 4.83, P = 0.002, η2p = 0.22 at distance and F(3.7, 62.8) = 6.42, P < 0.001, η2p = 0.27 at near). Post hoc test showed that at distance, the 0.00 D condition had statistically significantly better binocular VA than the +2.00 D simulated refractive imbalance condition (t(17) = 3.54, P = 0.002, d = 0.84). At near, the binocular VA at 0.00 D was significantly better than −2.00 D (t(17) = 4.38, P < 0.001, d = 1.03), −1.00 D (t(17) = 3.07, P = 0.007, d = 0.72), and +2.00 D (t(17) = 3.51, P = 0.003, d = 0.83).
Figure 1.
Mean binocular visual acuity for simulated refractive imbalance conditions. The graph shows binocular visual acuity. Orange and blue bars represent near visual acuity and distance visual acuity, respectively; error bars represent the standard error.
Figure 2 represents VA binocular summation results at near across refractive imbalance conditions. Binocular summation was seen in 72.2%, 38.9%, 72.2%, 66.7%, 44.4%, and 16.7% of participants for baseline and refractive imbalance conditions of −2.00 D, −1.00 D, 0.00 D, +1.00 D, and +2.00 D, respectively.
Figure 2.
Near VA binocular summation results for each condition. Six graphs show binocular VA (y-axis) and better eye VA (x-axis) in baseline and simulated refractive imbalance conditions as labeled. Unfilled circles are each individual's near visual acuity results. Filled circles represent the group average of the near visual acuity; error bars represent the standard error. Data points below the solid diagonal are indicative of binocular summation, data points on the diagonal show neither binocular summation or inhibition, and data points above the diagonal show binocular inhibition. Dotted lines are 0.02 logMAR difference from the solid line to assist in visualizing the data (one letter difference in VA chart).
There were no significant differences in binocular and monocular BV measures between baseline and the 0.00 D refractive imbalance condition after reading (all FDR-adjusted P > 0.05). Table 2 shows the mean and standard deviation of the clinical BV parameters at baseline and across simulated refractive imbalance conditions. Table 3 presents the heatmap where a higher percentage of participants not within ±1 SD of the expected mean values24 is indicated as a more saturated red and vice versa. Figure 3 shows the binocular FCC and MCC results for near distance.
Table 2.
Mean and Standard Deviation of Binocular Vision Parameters at Baseline and Across the Refractive Imbalance Conditions
| Visit 2: Refractive Imbalance Condition | |||||||
|---|---|---|---|---|---|---|---|
| Binocular Vision Test | Visit 1 Baseline | −2.00 D | −1.00 D | 0.00 D | +1.00 D | +2.00 D | P Value |
| Distance binocular vision parameters | |||||||
| Horizontal phoria (Δ) | −0.1 (2.3) | 1.9 (2.8) | 0.4 (3.4) | −0.3 (2.7) | 0.2 (3.3) | −0.1 (4.5) | 0.003 |
| NFR (break) (Δ) | 9.9 (3.3) | 7.2 (3.4) | 7.8 (2.4) | 9.3 (3.3) | 8.2 (2.8) | 8.0 (4.5) | 0.019 |
| NFR (recovery) (Δ) | 5.6 (2.4) | 3.3 (2.8) | 4.4 (2.1) | 5.4 (2.3) | 4.6 (2.6) | 3.7 (4.6) | 0.053 |
| PFR (break) (Δ) | 19 (6.9) | 18.4 (7.3) | 16.8 (7.0) | 17.4 (6.7) | 16.6 (6.9) | 16.1 (7.9) | 0.165 |
| PFR (recovery) (Δ) | 11.2 (6.2) | 13.3 (6.6) | 10.9 (6.2) | 11.4 (5.6) | 11.2 (5.9) | 9.1 (6.7) | 0.011 |
| Near binocular vision parameters | |||||||
| Near point of convergence (cm) | 6.1 (1.8) | 7.1 (3.3) | 6.7 (2.9) | 6.6 (3.1) | 7.3 (3.3) | 7.1 (3.7) | 0.141 |
| Binocular AA (D) | 10.5 (2.2) | 10.2 (4.0) | 10.4 (3.5) | 11.6 (3.0) | 11.5 (3.0) | 12.0 (3.7) | 0.029 |
| Accommodative facility (cpm) | 13.9 (3.8) | 15.6 (4.4) | 15.3 (3.8) | 14.2 (4.0) | 15.0 (3.9) | 14.9 (5.4) | 0.609 |
| Vergence facility (cpm) | 15.2 (3.9) | 14.9 (4.2) | 16.3 (3.4) | 16.8 (3.1) | 17.2 (3.9) | 15.7 (4.2) | 0.041 |
| Stereopsis (arcsecond) | 34.2 (20.1) | 185.0 (232.7) | 40.1 (24.8) | 34.3 (21.5) | 45.7 (35.1) | 98.5 (100.0) | 0.015 |
| Near horizontal phoria (Δ) | −5.1 (4.6) | −3.7 (4.9) | −4.7 (5.8) | −4.8 (5.3) | −5.3 (6.0) | −6.9 (7.4) | 0.013 |
| AC/A ratio | 2.7 (1.5) | 2.2 (1.5) | 3.1 (1.5) | 3.1 (1.4) | 2.6 (1.8) | 2.1 (1.3) | 0.014 |
| NFR (break) (Δ) | 19.1 (4.9) | 14.2 (5.3) | 18.1 (5.4) | 19.0 (5.9) | 19.0 (5.6) | 18.6 (8.9) | 0.002 |
| NFR (recovery) (Δ) | 13.5 (5.0) | 9.1 (5.0) | 10.8 (5.1) | 12.0 (5.5) | 13.2 (5.2) | 12.7 (7.1) | 0.036 |
| PFR (break) (Δ) | 23.7 (7.9) | 20.8 (7.7) | 23.3 (8.0) | 23.7 (7.6) | 20.4 (8.2) | 18.7 (9.2) | 0.004 |
| PFR (recovery) (Δ) | 16.7 (8.3) | 16.2 (7.0) | 15.8 (7.8) | 16.7 (7.4) | 14.4 (7.8) | 12.3 (7.6) | 0.018 |
| FCC – BE (D) | 0.1 (0.5) | 0.6 (1.1) | 0.5 (0.6) | 0.1 (0.5) | −0.1 (0.4) | −0.4 (0.6) | <0.001 |
| NRA – DE (D) | 2.7 (0.8) | 3.2 (1.2) | 2.8 (0.8) | 2.7 (0.6) | 2.5 (0.9) | 2.7 (0.8) | 0.021 |
| NRA – NDE (D) | 2.5 (0.9) | 2.5 (0.7) | 2.6 (0.7) | 2.5 (0.7) | 2.6 (0.7) | 2.5 (0.7) | 0.823 |
| NRA – BE (D) | 2.8 (0.8) | 3.5 (1.1) | 3.0 (0.9) | 2.8 (0.5) | 2.8 (0.7) | 2.7 (0.8) | 0.005 |
| PRA – DE (D) | −6.0 (2.3) | −4.5 (4.3) | −5.9 (2.4) | −6.2 (2.5) | −6.1 (2.5) | −6.6 (2.9) | 0.151 |
| PRA – NDE (D) | −6.3 (2.4) | −6.0 (2.3) | −6.3 (2.4) | −5.9 (2.4) | −6.3 (2.3) | −5.0 (4.4) | 0.368 |
| PRA – BE (D) | −5.4 (1.7) | −5.2 (2.2) | −5.6 (2.3) | −5.5 (2.3) | −5.6 (2.0) | −6.0 (3.0) | 0.110 |
Figures in parentheses stand for standard deviation. P values are from repeated-measures ANOVA analysis among refractive imbalance conditions. Nondominant eye monocular measures would be unchanged due to no manipulation of refraction for that eye alone.
AA, amplitude of accommodation; AC/A, accommodative convergence to accommodation; BE, both eyes; cpm, cycles per minute; DE, dominant eye; NDE, nondominant eye; NFR, negative fusional reserve; NRA, negative relative accommodation; PFR, positive fusional reserve; PRA, positive relative accommodation; Δ, prism diopter.
Table 3.
Heatmap of the Percentage of Participants Out of the Expected Binocular Vision Parameter Range at Baseline and Across the Refractive Imbalance Conditions
|
|---|
Values are presented as the percentage (%) of participants who are out of the reference binocular vision parameter range. Higher percentages are colored as darker red; the density of color is divided by a 10% gap. Nondominant eye monocular measures would be unchanged due to no manipulation of refraction for that eye alone. The binocular amplitude of accommodation reference was based on each participant's age.
Figure 3.
Binocular and unilateral (dominant eye versus nondominant eye) accommodative response (lag or lead) as assessed using the cross-cylinder test. The six graphs display the MCC of the dominant (y-axis) versus nondominant eye (x-axis) responses at baseline and five different simulated refractive imbalance conditions as labeled. Filled black circles represent the group average of the MCC response; error bars represent the standard error. The gray shaded areas show the reference ranges with ±1 standard deviation. The color of the unfilled circles indicates the binocular accommodative response (FCC result). Blue indicates the individual had a binocular lag, and red indicates a binocular lead of accommodation.
Contrast analysis revealed MCC in the dominant eye and binocular FCC had a downward linear trend from the −2.00 D to +2.00 D refractive imbalance condition (from greater stimulus to accommodation to lesser stimulus to accommodation) (F(1, 85) = 62.10, P < 0.001 in the dominant eye and F(1, 85) = 25.59, P < 0.001 binocularly). Negative relative accommodation in the dominant eye and binocularly also showed a downward linear trend, decreasing from the −2.00 D to +2.00 D condition (F(1, 85) = 4.15, P = 0.045 in the dominant eye and F(1, 85) = 7.80, P = 0.006 binocularly). Planned contrasts showed a U-shaped curve for stereopsis (F(1, 85) = 16.47, P < 0.001); the 0.00 D condition had best (lowest) stereoacuity, and stereoacuity worsened as the absolute value of the refractive imbalance increased. Planned contrasts showed an upside-down U-shaped curve for the accommodative convergence to accommodation ratio (F(1, 85) = 7.16, P = 0.009) and distance negative fusional reserve break values (F(1, 85) = 4.50, P = 0.037) also indicating worse function as the absolute value of the refractive imbalance increased. The contrast analyses for other BV parameters showed no trend with simulated refractive imbalance conditions (P > 0.05).
Figure 4 shows that refractive imbalance did not affect reading speed (F(3.1, 53) = 1.42, P = 0.25, η2p = 0.08) and comprehension (F(4, 64) = 0.44, P = 0.80, η2p = 0.02). There was no significant effect of delay between the reading and comprehension tasks on reading comprehension (F(4, 64) = 3.73, P = 0.07, η2p = 0.19).
Figure 4.
Mean reading comprehension score and reading speed for simulated refractive imbalance conditions. The left shows reading comprehension scores and the right presents reading speed in words per minute; error bars represent the standard error.
The average responses to items that assessed vision-related reading difficulty symptoms are presented in Figure 5. There were significant differences among simulated refractive imbalance conditions (P < 0.001). Post hoc tests showed that the 0.00 D condition had the lowest score (least symptoms) compared with other simulated refractive imbalance conditions in all items. There were no significant differences between the −1.00 D and +1.00 D conditions, between the −2.00 D and +2.00 D conditions, or for each item across refractive imbalance conditions (P > 0.05 at each item).
Figure 5.
Vision-related reading difficulty symptomatology scores for simulated refractive imbalance conditions. In each item, a higher score stands for a more negative response. Items 1, 2, 3, and 5 had four levels of answers: completely, very, slightly, and not at all. Item 4 had 0 minutes, 5 to 10 minutes, 15 to 30 minutes, and more than 30 minutes to 2 hours of options for answer (Supplementary Material S3). First, second, third, and fourth answer options in each question are converted as 0, 1, 2, and 3 points, respectively; error bars represent the standard error.
Discussion
This study described the impact of simulated refractive imbalance on VA, including binocular summation at near, BV status, reading performance (speed and comprehension), and vision-related reading difficulty symptoms in expert readers.
We found that simulated refractive imbalance impaired binocular VA both at near and distance; larger decrements of VA were observed with a greater magnitude of refractive imbalance. The current study agreed with findings from a study that recruited participants with habitual refractive imbalance, which showed poorer binocular distance VA with increasing refractive imbalance.36 Despite the statistically significant reductions of binocular distance and near VA under simulated refractive imbalance conditions, the averages of the VA were still better than “normal” (0.00 logMAR) in the current study, implying a subclinical worsening of vision (Fig. 1). The finding was similar to a previous study37 using ±0.50 D refractive imbalance conditions, where binocular VA remained better than 0.00 logMAR. Collectively, these results indicated that uncorrected refractive imbalance, either habitual or simulated, has a statistically significant negative influence on VA.
The dominant eye MCC and binocular FCC results at near distances changed in the same direction under simulated refractive imbalance conditions. The dominant eye MCC during nondominant eye occlusion and binocular FCC (both eyes open) responded to the simulated refraction condition with plus and minus ophthalmic powers with greater lag and lead of accommodation, respectively (Table 2 and Fig. 3). It may be inferred that the dominant eye had a stronger influence on the binocular accommodative response. Although theoretically, the visual system could have compared the accommodative effort required based on the dominant and nondominant eye and selected the response that would result in the minimal accommodative response,38,39 in the current study, the binocular response followed the dominant eye's accommodative response.
Considering that binocular accommodation was biased toward the dominant eye's accommodative response, the visual acuity in the nondominant eye would theoretically be more blurred due to the refractive imbalance being over the dominant eye. There could be three possible reasons that binocular VA was largely better than normal, although regarded as subjectively blurry by participants according to the vision-related reading difficulty questionnaire: (1) binocular summation assisted in improving VA binocularly16; (2) the more blurred image was suppressed,40 and attention was paid to the clearer image; and (3) depth of focus due to changed pupil size, affected by a triad of accommodation, vergence, and pupil response, assisted in maintaining binocular VA.41 From the current study, the first and second reasons may be possible as disruption of binocular summation and reduced stereoacuity results were seen with increasing refractive imbalance. However, it was unclear whether pupil size affected the VA result because pupil size was not measured.
In the current study, refractive imbalance additionally induced a change in vergence parameters in the participants. Myopic refractive imbalance (adding a plus ophthalmic lens), added to the dominant eye, shifted the distance and near heterophoria to become more exophoric (eyes turning out or more divergence), whereas hyperopic refractive imbalance (adding a minus ophthalmic lens) to the dominant eye resulted in a more esophoric posture (more convergence); larger shifts were observed with greater refractive imbalance. Our findings were in line with past studies, which have shown an association between binocular vision anomaly and habitual refractive imbalance,42 as well as a positive correlation between refractive imbalance magnitude and change in phoria. The most likely mechanism is the near triad response,41 whereby looking at a near object stimulates accommodation, convergence, and pupil constriction. In this case, when the stimulus to accommodation was increased to the dominant eye, this increased the stimulus to convergence (binocular response), resulting in a more esophoric response and vice versa for a reduction in the stimulus to accommodation.
Additionally, the findings in the current study suggested that in both simulated minus and plus refractive imbalance, the average fusional reserve decreased, and the percentage of participants who were outside clinically defined normal limits, based on the expected reference ranges,24 increased. Together, these poor vergence abilities with simulated refractive imbalance may be due to conflicting stimulation of the parts of the near triad response (refractive imbalance inducing more or relaxed accommodation in one eye that may affect pupil size and vergence, which are linked between the eyes) and/or differences of appearance of the same text between the eyes due to differential blur, resulting in difficulty in sensory fusion, which may reduce stereoacuity. In the current study, stereoacuity was poorer with increased simulated refractive imbalance, which was consistent with other habitual and simulated refractive imbalance studies.43,44 Therefore, the findings of the current study indicated that refractive imbalance may result in abnormalities of binocular function.
We found no significant association between simulated refractive imbalance and reading speed or comprehension in adult expert readers. Although there were differences in the length of reading texts, the reading text sets were not statistically significantly different in complexity based on Flesch score and the Flesch-Kincaid grade level, and they did not result in statistically significant differences in reading speed and comprehension in another pilot group of participants. This differs from a study in children that found smaller binocular imbalance asymmetries, like −0.75 D, were associated with a decrease in reading speed and comprehension ability.20 The potential differences between the current and previous study were the different maturity levels of participants and reading ability. Children, as learner readers, may have a lower level of linguistic processing while reading when compared to adults.45 This may result in refractive imbalance having a stronger negative influence on the reading process in children. Even though children have less blur detection than adults,46 visual noise has a greater negative effect on children's perception of contours than on adults’.47 Therefore, the blurred image resulting from simulated refractive imbalance may affect the ability to read the shapes of letters and words, thereby impacting reading speed and comprehension in children more than in adults. Experiments in adults with simulated bilateral defocus suggested that up to +2.00 D of refractive error did not reduce reading speed.48 In patients who habitually had refractive imbalance, reading speed was comparable to that of a control group who habitually wore full-distance refraction.49 Therefore, our finding of reading performance is contradictory with studies in children but is consistent with adult studies.
Short-term or working memory plays an important role in reading comprehension.50,51 The main processing mechanisms for learning and memory consist of encoding, storage, and retrieval.52 However, the mechanism for memory may be affected by two phenomena: fading away memory over time (i.e., decay)53 and displacing older information with new information (i.e., interference).54 In the current study, the study 1 group experienced both decay (30-minute time delay) and interference (by conducting the binocular vision assessment) between reading the text and solving the reading comprehension questionnaires, whereas the study 2 group performed the comprehension questionnaire immediately after reading the text. The study 1 group had lower comprehension scores than the study 2 group, although it failed to reach significance (P = 0.08), which was in agreement with a previous study showing reading comprehension between immediate and 30-minute delay was not significantly different with or without a noisy (interference) condition.55 Another study, with much longer delay recall times over 24 hours, found that delayed time reduced reading comprehension scores.56 Therefore, the 30-minute delay that occurred for the study 1 group in the current study did not significantly affect reading comprehension.
Vision appeared to be subjectively blurrier under refractive imbalance conditions according to the symptomatology questionnaire results. However, clinically, the participants had good binocular VA results (better than 0.00 logMAR). This indicated that participants must have achieved their good visual acuity through interpretation of the blurred fused image, increasing attention to the eye with the clearer image and decreasing attention and/or suppressing information from the eye with the poorer image, or intensified concentration to fuse the images despite conflicting stimuli in vergence and accommodation. Furthermore, participants had difficulty answering questions about the text and concentrating on the text while reading under refractive imbalance conditions, but the reading speed and comprehension results were not significantly different across conditions. These findings suggested that additional cognitive effort (e.g., concentration) was being expended to read and maintain reading speed and comprehension at the expense of visual comfort and the ability to continue reading. Hence, although the refractive imbalance did not appear to affect the objectively measured factors of reading speed and comprehension, as well as relatively good binocular VA, refractive imbalance negatively affected all measured vision-related reading difficulty symptoms; therefore, as a clinical extension, full correction of refractive imbalance is recommended.
A limitation of the current study was that simulating refractive imbalance conditions may have measured effects that differ from individuals who habitually have refractive imbalance and who may have adapted or be unaware that their vision is imbalanced. However, by using simulation, it could have important advantages of removing the effects of amblyopia and aniseikonia, which can be associated with habitual refractive imbalance. Another limitation was that the duration of the reading task may not have been sufficiently long enough to result in decrements of reading speed and comprehension. The symptomatology questionnaire answered by the study 2 group participants indicated that, on average, they would not be happy to read for longer than a further 5 to 10 minutes with refractive imbalance. This suggests that longer reading times may result in greater decrements of reading performance. Many previous studies investigating the relationship between near work and binocular vision status used at least 20 minutes of near work,57–60 while the current study used approximately 3 minutes of reading duration. Although the current study found statistically significant differences in some binocular vision parameters, a longer duration of reading would provide greater insight into the results; therefore, future studies could investigate longer reading durations. Although there was random ordering of reading text sets, different lengths of the sets resulted in different reading times, which may potentially affect measured outcomes. A pilot study (see Supplementary Material S1) found no statistical difference in reading speed, comprehension, and vision-related reading difficulty symptoms across the text sets, but it is unclear whether the differing text lengths impacted binocular vision measurements. This study did not investigate adding refractive imbalance to the nondominant eye, so it is unclear whether the binocular accommodative response would follow the dominant eye under those conditions, although it is likely to be true.
In conclusion, the study demonstrated that compared with best-corrected refraction, simulated refractive imbalance with a −2.00 D to +2.00 D difference between the eyes was associated with statistically significant changes in binocular vision status. Although there was a statistically significant reduction in binocular VA with refractive imbalance, binocular VA was still better than 0.00 logMAR. Reading speed and comprehension were not significantly affected by simulated refractive imbalance, but vision-related reading difficulty symptoms were worse with greater refractive imbalance. Overall, full correction of refractive imbalance is beneficial to reading, particularly through decreasing discomfort and increasing ability to continue reading.
Supplementary Material
Acknowledgments
The authors thank the participants for their participation and Lisa Kong for help with data collection.
Disclosure: T. Lee, None; M. Leung, None; J.J.A. van Boxtel, None; M.Y. Boon, None
References
- 1. Resnikoff S, Pascolini D, Mariotti SP, Pokharel GP. Global magnitude of visual impairment caused by uncorrected refractive errors in 2004. Bull World Health Organ. 2008; 86(1): 63–70. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. World Health Organization. Report of the 2030 Targets on Effective Coverage of Eye Care. Geneva, Switzerland: World Health Organization; 2022. [Google Scholar]
- 3. Guzowski M, Fraser-Bell S, Rochtchina E, Wang JJ, Mitchell P. Asymmetric refraction in an older population: the blue mountains eye study. Am J Ophthalmol. 2003; 136(3): 551–553. [DOI] [PubMed] [Google Scholar]
- 4. Wong TY, Foster PJ, Hee J, et al.. Prevalence and risk factors for refractive errors in adult Chinese in Singapore. Invest Ophthalmol Vis Sci. 2000; 41(9): 2486–2494. [PubMed] [Google Scholar]
- 5. Krishnaiah S, Srinivas M, Khanna RC, Rao GN. Prevalence and risk factors for refractive errors in the South Indian adult population: the Andhra Pradesh Eye disease study. Clin Ophthalmol. 2009; 3: 17–27. [PMC free article] [PubMed] [Google Scholar]
- 6. Antón A, Andrada MT, Mayo A, Portela J, Merayo J. Epidemiology of refractive errors in an adult European population: the Segovia study. Ophthalmic Epidemiol. 2009; 16(4): 231–237. [DOI] [PubMed] [Google Scholar]
- 7. Khatri B, Shrestha R, Suwal R, et al.. Utilisation of eye health services and compliance with spectacles wear among community school adolescents: a mixed-methods study from Bagmati province of Nepal. BMJ Open. 2024; 14(8): e087287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Häkkinen L. Vision in the elderly and its use in the social environment. Scand J Soc Med Suppl. 1984; 35: 5–60. [PubMed] [Google Scholar]
- 9. Dadeya S, Kamlesh SF. The effect of anisometropia on binocular visual function. Indian J Ophthalmol. 2001; 49(4): 261–263. [PubMed] [Google Scholar]
- 10. Tomaç S, Birdal E. Effects of anisometropia on binocularity. J Pediatr Ophthalmol Strabismus. 2001; 38(1): 27–33. [DOI] [PubMed] [Google Scholar]
- 11. Heo J, Yoo K. Effect of experimentally induced anisometropia on binocular vision. J Korean Ophthalmol Soc. 1999; 40: 3468–3473. [Google Scholar]
- 12. Atchison DA, Lee J, Lu J, et al.. Effects of simulated anisometropia and aniseikonia on stereopsis. Ophthalmic Physiol Opt. 2020; 40(3): 323–332. [DOI] [PubMed] [Google Scholar]
- 13. Simpson T. The suppression effect of simulated anisometropia. Ophthalmic Physiol Opt. 1991; 11(4): 350–358. [PubMed] [Google Scholar]
- 14. Ding J, Klein SA, Levi DM. Binocular combination in abnormal binocular vision. J Vis. 2013; 13(2): 14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Heravian JS, Jenkins TC, Douthwaite WA. Binocular summation in visually evoked responses and visual acuity. Ophthalmic Physiol Opt. 1990; 10(3): 257–261. [PubMed] [Google Scholar]
- 16. Home R. Binocular summation: a study of contrast sensitivity, visual acuity and recognition. Vis Res. 1978; 18(5): 579–585. [DOI] [PubMed] [Google Scholar]
- 17. Woodman W, Young M, Kelly K, Simoens J, Yolton RL. Effects of monocular occlusion on neural and motor response times for two-dimensional stimuli. Optom Vis Sci. 1990; 67(3): 169–178. [DOI] [PubMed] [Google Scholar]
- 18. Heller D, Radach R. Eye movements in reading: are two eyes better than one? In: Becker W, Deubel H, Mergner T, eds. Current Oculomotor Research: Physiological and Psychological Aspects. Boston, MA: Springer; 1999: 341–348. [Google Scholar]
- 19. Neale MD. Neale Analysis of Reading Ability: Reader. Melbourne, VIC: ERIC; 1999. [Google Scholar]
- 20. Narayanasamy S, Vincent SJ, Sampson GP, Wood JM. Simulated hyperopic anisometropia and reading, visual information processing, and reading-related eye movement performance in children. Invest Ophthalmol Vis Sci. 2014; 55(12): 8015–8023. [DOI] [PubMed] [Google Scholar]
- 21. Buczkowska H, Miskowiak B. Comparison of reading speed, phonological decoding, and comprehension in the group of children with anisometropic amblyopia and control group. Optica Applicata. 2017; 47(3): 351–362. [Google Scholar]
- 22. Reindel W, Zhang L, Chinn J, Rah M. Evaluation of binocular function among pre- and early-presbyopes with asthenopia. Clin Optom. 2018; 10: 1–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Evans BJ. Pickwell's Binocular Vision Anomalies e-Book. Philadelphia, PA: Elsevier Health Sciences; 2021. [Google Scholar]
- 24. Scheiman M, Wick B. Clinical Management of Binocular Vision: Heterophoric, Accommodative, and Eye Movement Disorders. Philadelphia, PA: Lippincott Williams & Wilkins; 2008. [Google Scholar]
- 25. Mapp AP, Ono H, Barbeito R. What does the dominant eye dominate? A brief and somewhat contentious review. Perception Psychophysics. 2003; 65(2): 310–317. [DOI] [PubMed] [Google Scholar]
- 26. Linke SJ, Richard G, Katz T. Prevalence and associations of anisometropia with spherical ametropia, cylindrical power, age, and sex in refractive surgery candidates. Invest Ophthalmol Vis Sci. 2011; 52(10): 7538–7547. [DOI] [PubMed] [Google Scholar]
- 27. Hashemi H, Khabazkhoob M, Lança C, Emamian MH, Fotouhi A. Prevalence of anisometropia and its associated factors in school-age children. Strabismus. 2024; 32: 1–10. [DOI] [PubMed] [Google Scholar]
- 28. Krarup TG, Nisted I, Christensen U, Kiilgaard JF, La Cour M. The tolerance of anisometropia. Acta Ophthalmol. 2020; 98(4): 418–426. [DOI] [PubMed] [Google Scholar]
- 29. Rouse MW, Borsting EJ, Lynn Mitchell G, et al.. Validity and reliability of the revised convergence insufficiency symptom survey in adults. Ophthalmic Physiol Opt. 2004; 24(5): 384–390. [DOI] [PubMed] [Google Scholar]
- 30. Subhash S, Cudney EA. Gamified learning in higher education: a systematic review of the literature. Comput Hum Behav. 2018; 87: 192–206. [Google Scholar]
- 31. Flesch R. A new readability yardstick. J Appl Psychol. 1948; 32(3): 221–233. [DOI] [PubMed] [Google Scholar]
- 32. Flesch R. How to write plain English. 1979, https://pages.stern.nyu.edu/∼wstarbuc/Writing/Flesch.htm. Accessed February 5, 2016. [Google Scholar]
- 33. Legge GE, Bigelow CA. Does print size matter for reading? A review of findings from vision science and typography. J Vis. 2011; 11(5): 8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34. Jamovi. The Jamovi project 2020 (Version 1.2) [Computer software], https://www.jamovi.org. Accessed January 29, 2023.
- 35. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995; 57(1): 289–300. [Google Scholar]
- 36. Levi DM, McKee SP, Movshon JA. Visual deficits in anisometropia. Vis Res. 2011; 51(1): 48–57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37. Atchison DA, Schmid KL, Edwards KP, Muller SM, Robotham J. The effect of under and over refractive correction on visual performance and spectacle lens acceptance. Ophthalmic Physiol Opt. 2001; 21(4): 255–261. [DOI] [PubMed] [Google Scholar]
- 38. Koh LH, Charman WN. Accommodative responses to anisoaccommodative targets. Ophthalmic Physiol Opt. 1998; 18(3): 254–262. [PubMed] [Google Scholar]
- 39. Vincent SJ, Collins MJ, Read SA, et al.. The short-term accommodation response to aniso-accommodative stimuli in isometropia. Ophthalmic Physiol Opt. 2015; 35(5): 552–561. [DOI] [PubMed] [Google Scholar]
- 40. Shors TJ, Wright K, Greene E. Control of interocular suppression as a function of differential image blur. Vis Res. 1992; 32(6): 1169–1175. [DOI] [PubMed] [Google Scholar]
- 41. Fincham EF. The accommodation reflex and its stimulus. Br J Ophthalmol. 1951; 35(7): 381. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42. O'Donoghue L, McClelland JF, Logan NS, Rudnicka AR, Owen CG, Saunders KJ. Profile of anisometropia and aniso-astigmatism in children: prevalence and association with age, ocular biometric measures, and refractive status. Invest Opthalmol Vis Sci. 2013; 54(1): 602. [DOI] [PubMed] [Google Scholar]
- 43. Brooks SE, Johnson D, Fischer N. Anisometropia and Binocularity. Ophthalmology. 1996; 103(7): 1139–1143. [DOI] [PubMed] [Google Scholar]
- 44. Singh P, Bergaal SK, Sharma P, Agarwal T, Saxena R, Phuljhele S. Effect of induced anisometropia on stereopsis and surgical tasks in a simulated environment. Indian J Ophthalmol. 2021; 69(3): 568–572. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45. Aaronson D, Ferres S. Reading strategies for children and adults: a quantitative model. Psychol Rev. 1986; 93(1): 89–112. [PubMed] [Google Scholar]
- 46. Roberts TL, Stevenson SB, Benoit JS, Manny RE, Anderson HA. Blur detection, depth of field, and accommodation in emmetropic and hyperopic children. Optom Vis Sci. 2018; 95(3): 212–222. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47. Kovács I, Kozma P, Fehér A, Benedek G. Late maturation of visual spatial integration in humans. Proc Natl Acad Sci USA. 1999; 96(21): 12204–12209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48. Chung STL, Jarvis SH, Cheung S-H. The effect of dioptric blur on reading performance. Vis Res. 2007; 47(12): 1584–1594. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49. Kelly KR, Jost RM, De La, Cruz A, et al.. Slow reading in children with anisometropic amblyopia is associated with fixation instability and increased saccades. J Am Assoc Pediatr Ophthalmol Strabismus. 2017; 21(6): 447–451.e441. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50. Seigneuric A, Ehrlich M-F, Oakhill JV, Yuill NM. Reading Writing. 2000; 13(1/2): 81–103. [Google Scholar]
- 51. Peng P, Barnes M, Wang C, et al.. A meta-analysis on the relation between reading and working memory. Psychol Bull. 2018; 144(1): 48. [DOI] [PubMed] [Google Scholar]
- 52. Poeppel D, Mangun GR, Gazzaniga MS. The Cognitive Neurosciences. Cambridge, MA: MIT Press; 2020. [Google Scholar]
- 53. Brown J. Some tests of the decay theory of immediate memory. Q J Exp Psychol. 1958; 10(1): 12–21. [Google Scholar]
- 54. McConnell J, Quinn J. Interference in visual working memory. Q J Exp Psychol A. 2000; 53(1): 53–67. [DOI] [PubMed] [Google Scholar]
- 55. Brännström KJ, Waechter S. Reading comprehension in quiet and in noise: effects on immediate and delayed recall in relation to tinnitus and high-frequency hearing thresholds. J Am Acad Audiol. 2018; 29(06): 503–511. [DOI] [PubMed] [Google Scholar]
- 56. Gambrell LB, Pfeiffer WR, Wilson RM. The effects of retelling upon reading comprehension and recall of text information. J Educ Res. 1985; 78(4): 216–220. [Google Scholar]
- 57. Golebiowski B, Long J, Harrison K, Lee A, Chidi-Egboka N, Asper L. Smartphone use and effects on tear film, blinking and binocular vision. Curr Eye Res. 2020; 45(4): 428–434. [DOI] [PubMed] [Google Scholar]
- 58. Lee J-W, Cho HG, Moon B-Y, Kim S-Y, Yu D-S. Effects of prolonged continuous computer gaming on physical and ocular symptoms and binocular vision functions in young healthy individuals. PeerJ. 2019; 7: e7050. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59. Talens-Estarelles C, Cerviño A, García-Lázaro S, Fogelton A, Sheppard A, Wolffsohn JS. The effects of breaks on digital eye strain, dry eye and binocular vision: testing the 20-20-20 rule. Contact Lens Anterior Eye. 2023; 46(2): 101744. [DOI] [PubMed] [Google Scholar]
- 60. Yu H-R, Choi A, Park M, Kim SR. Changes of binocular vision function in eyes with normal and abnormal visual function according to reading devices. J Korean Ophthalmic Opt Soc. 2019; 24(2): 143–152. [Google Scholar]
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