Changes in corneal astigmatism and near heterophoria after smartphone use while walking and sitting.

BACKGROUND/AIMS: Smartphone use has become an indispensable part of our daily life. The handy design and powerful processor allow smartphone users to perform diversified tasks even when walking. This study aimed to investigate and compare the optical aftereffect and vergence adaptation of using a smartphone while walking and sitting.
METHODS: Twenty-nine young healthy adults (aged 19 to 24 years old) with normal binocular and accommodative functions were recruited. Participants were asked to watch a movie for 30 minutes using a smartphone while either walking on a treadmill or sitting on a chair. Corneal aberrations and near heterophoria were measured before and after smartphone use by a corneal topographer and modified Thorington heterophoria test, respectively.
RESULTS: Using the smartphone while walking induced a change in corneal H/V astigmatism, becoming 0.11±0.03 μm less negative (two-way ANOVA repeated measures, Bonferroni post-hoc test, p = 0.001). This optical aftereffect was significantly higher than after smartphone use while sitting by 0.10±0.03 μm (paired t-test, p = 0.003). Although smartphone use did not result in a significant change in near heterophoria (Bonferroni post-hoc test, p > 0.15), the vergence adaptation showed relatively more eso- or less exo-deviation by 0.79±0.36Δ in the walking than the sitting condition (paired t-test, p = 0.037).
CONCLUSIONS: Eyecare practitioners should be cautious of the potential optical after effect and vergence adaptation after prolonged smartphone usage.

Introduction

In this digital era, using a smartphone has become an indispensable part of our daily life. The number of smartphone users is growing dramatically worldwide, reaching 3.5 billion users by 2020 [1]. The powerful processor and well-designed mobile apps allow diversified functions. Users can enjoy video streaming, play games, learn from diverse resources, engage in social media communication, and perform many other activities all with a single device. Inevitably, these robust features induce users to spend more time on their mobile devices. For example, in Hong Kong, where over 90% of adults own at least one smartphone [2], average use of mobile devices is 2.4 hours each day, with 20% of users spending more than 4 hours per day [3]. Unlike traditional computers that can only be used at a fixed working station, the design of smartphones allows owners to use their mobile devices almost everywhere, even while they are walking.

Although smartphones are hugely productive tools that bring great convenience to our daily life, using a smartphone while walking can pose considerable dangers. According to a recent survey conducted by the American Academy of Orthopaedic Surgeons [4], about one-third of the smartphone users frequently use their smartphones while walking for non-speech activities (such as reading emails/websites, texting, playing games, or taking selfies). Of these users, 26% had encountered walking incidents, ranging from bumping into obstacles without injuries to sprains or fractures. Previous studies have shown that using a mobile device while walking alters gait kinematics [5], provokes risky street-crossing behaviors [6], and reduces the awareness of roadside surroundings [7]. Despite this variety of hazards associated with smartphone use, how sitting and walking affects our vision during smartphone use remains elusive.

The overuse of smartphones substantially increases the risk for digital eye strain (or computer vision syndrome), which has become a recognized global health problem [8, 9]. A recent survey of over 10,000 US adults revealed that 65% of respondents experienced symptoms related to the use of digital devices [10]. Digital eye strain can be categorized into internal and external symptoms [11]. Internal symptoms, including blurred vision, diplopia, eyestrain, and headache, are linked to the stress on the refractive and binocular vision systems of the eye, whilst external symptoms, including excessive tearing, dryness, burning, and irritation, are closely related to the dry eye syndrome. While these symptoms are usually transient, they can frequently cause a significant visual disturbance to individuals.

Because of the reduced screen dimensions and small font size, a smartphone is usually used at a short viewing distance, on average 36.3 cm for texting and 32.2 cm for internet viewing [12], posing substantial stress to the optical and fusional vergence systems of the eye. For instance, prolonged near-work, using either video display terminals or hard-copy reading materials, leads to a transient increase in both against-the-rule corneal astigmatism (negative cylindrical axis at 90 degrees) [13-15] and myopia [16, 17], which could temporally degrade both distance and near vision. Short-term adaptation of functional vergence to near tasks also shifts near heterophoria [18-21], with the magnitude of deviation associated with the subjective report of visual fatigue [19]. These transient changes in optical and vergence systems of the eye can vary with the gaze position. Collins et al. [15] and Buehren et al. [14] reported that near tasks that required a more downward gaze induced more against-the-rule corneal astigmatism, probably due to the increased eyelid pressure exerted onto the cornea. In addition, the resting position of tonic vergence varies with the inclination angle of the eye, as a downward gaze usually results in a near shift of heterophoria [22, 23]. Raap and Ebenholtz [24] also found that eye movement could prevent adaptation of the fusional vergence system to convergent stimuli (i.e., the stimulation of inward movement of both eyes, such as near tasks). It is worth noting that contrary to sitting, walking involves continuous movement of the gaze position to coordinate with head and body motions [25]. Thus, this study hypothesized that using smartphones while sitting and walking might place different stress on the visual systems and affect the optics and fusional vergence of the eye.

In this study, we investigated the effect of smartphone use on optical qualities and binocular functions of the eye. Specifically, we measured changes in corneal astigmatism and near heterophoria after 30 minutes of smartphone use between two experimental conditions: while walking on a treadmill or sitting on a chair. This study provides additional evidence on the potential ocular hazards of smartphone usage under different viewing conditions.

Materials and methods

Twenty-nine young, healthy Chinese adults (age: 18–24 years old) with normal binocular and accommodative functions participated in this study. All participants had spherical-equivalent refractive errors of +4.00DS to -6.00DS and astigmatism of 1.50DC or less, with corrected visual acuity at distance better than logMAR 0 in either eye. None had more than 1D of anisometropia. They were all free from strabismus, amblyopia, and ocular disease, and had no history of ocular surgeries. This study complied with the Declaration of Helsinki and was approved by the Human Subjects Ethics Committee of the Hong Kong Polytechnic University (HSEARS20150715001). Written informed consent was obtained from each eligible participant after explaining the experimental procedures.

Before starting the study, all participants underwent an eye examination to determine their refractive status and ocular health. Non-cycloplegic subjective refraction, using maximum-plus-maximum-acuity as the endpoint [26], was conducted to measure their refractive errors. Participants were required to wear their habitual spectacle corrections when either principal power meridian was more than 0.75 D. If the corrective power of their spectacle lenses deviated more than 0.50 D from their subjective refraction, they were advised to obtain a new pair of spectacles. Otherwise, they were excluded from this study. None of the participants was a regular contact lens wearer. A list of standard clinical procedures was also conducted to rule out binocular vision and ocular accommodation anomalies: cover test for distance and near dissociated heterophoria, Royal Air Force rule for near point of convergence and amplitude of accommodation, ±2D flipper for accommodative facility, and Risley prism on phoropter for distance and near fusional vergence reserve. Binocular and accommodative functions which exceeded 95% confidence intervals (CI) of the age norm were considered as abnormal [27]. Eligible participants were invited to complete the following procedures.

Experimental protocols

This study investigated the effect of using a smartphone on the corneal optical quality and binocular vision while either walking or sitting and was conducted over two separate visits. The order of walking and sitting conditions was assigned randomly. Each visit started at about the same time of the day (± 2 hours) to avoid potential diurnal variation of corneal biometry [28]. Before and after the smartphone use in each visit, participants first underwent the near dissociated heterophoria test, followed by corneal aberrometry measurement (see detailed procedures below). These procedures took less than five minutes. The near heterophoria was determined before the corneal aberrometry because the aberrometer blocks one eye during the measurement, which could have interfered with the vergence system following smartphone use.

At each visit, participants were first seated in a dark room for three minutes to dissipate any transient changes in accommodation and vergence before starting the measurements [29, 30]. The experiment began with baseline measurements of near heterophoria and corneal aberrometry. The participants, wearing any habitual spectacles, used a smartphone (LG G3 Stylus D690N, Republic of Korea) to watch a Korean variety show called “Running Man”, a popular foreign TV program in Hong Kong, for 30 minutes with Chinese subtitle (subtitle’s size: ~ 3mm). None of the participants knew Korean, and reading the subtitle was necessary. The screen (size: 5.5 inches; weight 163 g; resolution: 540 x 960 pixels) was held horizontally to maximize the display dimension, with the luminance set to its maximum level (~ 570 cd/m2 for a white background). The ambient room lighting was maintained at about 300 lux. Participants were either sitting on a height-adjustable office chair or walking on a treadmill (Model: Cadence 4.9 Weslo, West Logan, UT) while using the smartphone. The speed of the treadmill was set at 0.7 m/s with an inclination angle of 10 degrees. For safety reasons, a console key was attached to participants’ clothes. In an emergency, the console key would be detached to slow down and stop the walking belt, although this never occurred during the study. An examiner stood nearby to monitor the whole process. Immediately after 30 minutes of smartphone use, near heterophoria and corneal aberration measurements were repeated.

Corneal aberration measurement

Corneal topography was measured by an i.Profiler aberrometer (Carl Zeiss Vision, German), which incorporates a Placido-disk based videokeratoscope (number of rings: 22; up to 3,425 measuring points). Once the instrument was aligned with the pupil center, it automatically captured five consecutive corneal topographies and averaged the wavefront data to reduce any random measurement errors. The whole process took about 1–2 minutes. The corneal wavefront aberrations were derived from a 5-mm pupil diameter using Zernike polynomials up to the 7th radial order. The lower-order corneal aberrations, i.e., oblique astigmatism and H/V astigmatism, were averaged for data analysis. Higher-order corneal aberrations were excluded from the data analysis because they contributed to less than 10% of the total corneal aberration and were likely to have minimal clinical implications on visual quality. This study only determined corneal, but not ocular aberrations, for two reasons. Firstly, the study measured aberrations under a natural pupil without pharmacological dilation, and thus, thirteen participants (i.e., about 45% of our sample) could not achieve a 5 mm or larger pupil diameter. Secondly, because aberrometry was performed without cycloplegia, the aberrometer might have stimulated proximal accommodation and affected the internal (or lenticular) and overall aberrations of the eye. Nevertheless, because ocular astigmatism mostly originates from the cornea [31, 32], and the near-work induced change in ocular aberrations was highly correlated with the changes in corneal aberrations [14], the measurement of corneal astigmatism should, at least in part, reflect the changes in the overall optical quality of the eye after smartphone use.

To aid in the interpretation of the corneal H/V astigmatism, Z(2, 2), and oblique astigmatism, Z(2, -2), we also presented corneal astigmatism in diopter units by converting the Zernike coefficients ( and ) to power vectors (J0 and J45) [33]. where r is the pupil radius. The J0 and J45 are the astigmatic components with horizontal/vertical and oblique axes, respectively, and can be converted to the cylindrical form (Cyl) for a correcting lens as follow [34].

Near heterophoria measurement

The modified Thorington method was used to measure near dissociated heterophoria because the procedure is fast and straightforward with good inter-examiner repeatability [35-38]. During the measurement, a Maddox rod with the striations oriented horizontally was placed in front of the right eye to create a vertical striated light. Participants were asked to fixate at a light spot located at the center of a Bernell Muscle Imbalance Measure (MIM) card [35] at 40 cm and report the lateral displacement of the vertical striated light. They were reminded to always keep the scales of the MIM card clear throughout the whole process. The reported scales represent the near dissociated heterophoria.

Results

Demographic and baseline information

Participants’ demographic information, baseline corneal aberrations, and near heterophoria are summarized in Table 1. All participants had a negative corneal H/V astigmatism with an average of (mean±SE) -0.86±0.09 μm, equivalent to about +0.67 D of J0 astigmatism [33]. The magnitude of corneal oblique astigmatism was relatively low (0.09±0.05 μm, equivalent to about -0.07 D of J45 astigmatism), about 9.5 times smaller than the corneal H/V astigmatism. The majority of our participants exhibited exophoria (n = 26, 5.46±0.71Δ exophoria), one had orthophoria, and two had esophoria (1.5Δ and 2.5Δ esophoria, respectively). Table 2 summarizes the changes in corneal astigmatism and near heterophoria before and after smartphone use.

Table 1

Demographic and baseline information.

	Mean (95% confidence intervals)
Age	21.5 y (22.03, 20.97)
Gender	40% female
Spherical Equivalent	-2.67 DS (-3.50, -1.84)
Astigmatism	0.57 DC (0.38, 0.76)
Oblique Astigmatism Z(2, -2)	0.090 μm (0.043, 0.137)
H/V Astigmatism Z(2, 2)	-0.86 μm (-0.76, -0.95)
Near Heterophoria	4.76Δ Exophoria (4.01, 5.50)

Table 2

Summary of changes in corneal astigmatism and near heterophoria after 30-minute smartphone use while walking and sitting.

		Walking	Sitting
Oblique Astigmatism Z(2, -2) (μm)	Pre	0.070±0.045	0.110±0.052
	Post	0.058±0.048	0.073±0.049
H/V Astigmatism Z(2, 2) (μm)	Pre	-0.883±0.097*	-0.831±0.092
	Post	-0.769±0.095*	-0.816±0.096
Near Heterophoria (Δ)	Pre	4.72±0.77	4.79±0.77
	Post	4.37±0.71†	5.24±0.73†

Two-way ANOVA repeated measures was used to examine the effect of time and experimental conditions on corneal astigmatism and near heterophoria. There were statistically significant interactions between the effects of time and experimental conditions on H/V astigmatism (F(1, 28) = 8.09, p = 0.008) and near heterophoria (F(1, 29) = 4.78, p = 0.037).

Bonferroni post-hoc test: Pre vs Post * p = 0.001; Walking vs Sitting † p = 0.009.

Changes in corneal astigmatism

The results showed that smartphone use while walking for only 30 minutes significantly increased corneal H/V astigmatism, but was not significant for use while sitting (Fig 1, two-way ANOVA repeated measures: experimental conditions X time interaction: F(1, 28) = 8.09, p = 0.008). Compared with the baseline, the corneal H/V astigmatism after walking using the smartphone for 30 minutes became less negative by 0.11±0.03 μm (Fig 1B, Bonferroni post-hoc test, t = 3.80, p = 0.001). However, in the sitting condition, the change in corneal H/V astigmatism between the baseline and post-smartphone use was not statistically significant (t = 0.65, p = 0.53).

Fig 1

Optical aftereffects following 30 minutes of smartphone use.

A) Results for subject S01: The change in corneal wavefront was more obvious after smartphone use while walking than sitting. B) Corneal H/V astigmatism: The corneal H/V astigmatism became significantly less negative after smartphone use while walking, but no significant change was found while sitting. C) Corneal H/V astigmatism: The change in H/V astigmatism was significantly more positive while walking than sitting. D & E) Corneal oblique astigmatism: The optical aftereffect for the corneal oblique astigmatism was not statistically significant, and no significant difference in the change in oblique astigmatism was found between groups. Red symbols: Walking; Blue symbols: Sitting. Bonferroni post hoc test or paired t-test: ** p < 0.01.

Comparison of the two experimental conditions showed that corneal H/V astigmatism at the baseline was slightly more negative (0.05±0.03 μm) in the walking than the sitting condition (Fig 1B, Bonferroni post-hoc test, t = 1.86, p = 0.074), but after using the smartphone for 30 minutes, corneal H/V astigmatism was 0.05±0.02 μm more positive in the walking than the sitting condition (t = 2.04, p = 0.051). However, both comparisons failed to reach statistical significance.

To better understand the difference between the two experimental conditions, change in corneal H/V astigmatism before and after smartphone use (i.e., post–baseline) was compared and was found to be significantly more positive while walking than sitting (Fig 1C, paired t-test, t = 3.31, p = 0.003).

The effect of smartphone use on the corneal oblique astigmatism was not statistically significant, neither during walking nor sitting (Fig 1D, experimental conditions: F(1, 28) = 4.06, p = 0.053; time: F(1, 28) = 3.42, p = 0.075; interaction: F(1, 28) = 0.98, p = 0.330). The change in corneal oblique astigmatism (i.e., post–baseline) was also not significantly different between the two experimental conditions (Fig 1E, paired t-test, t = 1.77, p = 0.09).

Changes in near heterophoria

Near heterophoria showed a different pattern of vergence adaptation between the two experimental conditions (Fig 2A, two-way ANOVA repeated measures: experimental condition X time interaction: F(1, 29) = 4.78, p = 0.037). While near heterophoria at the baseline was comparable between the two experimental conditions (Bonferroni post-hoc test, t = 0.17, p = 0.863), the near heterophoria after 30 minutes of smartphone use showed 0.86±0.30Δ less exo-deviation (i.e., the eyes tended to turn out less) while walking than sitting (t = 2.83, p = 0.009). Comparison of the baseline and post-smartphone use sessions revealed that the eye tended to show more exo-deviation while sitting and less exo-deviation while walking after using the smartphone. However, none of these changes reached statistical significance (both t < 1.38, p > 0.15).

Fig 2

Vergence adaptation following 30 minutes of smartphone use.

A) In the post-smartphone use session, near heterophoria showed significantly less exo-deviation (i.e., less positive) after walking than sitting, while no significant difference was found at the baseline. B) Change in near heterophoria showed significantly less exo-deviation (or more eso-deviation) for walking than sitting. Positive: Exo-deviation; negative: Eso-deviation. Red symbols: Walking; Blue symbols: Sitting. Bonferroni post hoc test: ** p < 0.01, paired t-test: * p < 0.05.

Changes in near-heterophoria (i.e., post–baseline) between the two experimental conditions were also compared. Smartphone use while walking resulted in the eyes tending to shift to more eso- or less exo-deviation than when sitting (Fig 2B, paired t-test, t = 2.19, p = 0.037).

Discussion

With improvements in technology, the smartphone has become more portable and powerful, enabling users to perform diversified tasks in different environments. This study compared the optical aftereffect and vergence adaptation of using a smartphone while walking and sitting. The findings revealed that using a smartphone while walking resulted in a less negative corneal H/V astigmatism, and this change was significantly higher than that observed while sitting. The near heterophoria after walking with smartphone use was also more esophoric (or less exophoric) than sitting.

This study confirms that intensive near work reduced with-the-rule or induced against-the-rule corneal astigmatism [13-15]. When performing near tasks, the palpebral aperture usually becomes narrower, increasing the pressure the eyelid exerts onto the cornea and alters corneal toricity [13]. The magnitude of corneal astigmatic changes appears to be associated with the gaze position: a downward gaze, such as reading and performing microscopy, induces more against-the-rule astigmatism than a forward gaze, such as using computers [15]. It was observed that participants tended to have a more downward gaze when using smartphones while walking than when sitting. The change in gaze direction is probably an involuntary reflex to ensure safety by increasing the visual field of the walking path. This change to a downward gaze may explain the difference in the optical aftereffects between walking and sitting while using a smartphone (Fig 1A). However, other factors, such as the extraocular muscle forces generated during convergence [39], inter-blinking duration [40], and magnitude of accommodation [41], could also contribute to the variation of corneal shape and aberrations after smartphone uses.

The average change in corneal H/V astigmatism after walking use was equivalent to about 0.18 DC against-the-rule astigmatism. In this study, eleven participants showed >0.25 DC of induced against-the-rule astigmatism (H/V astigmatism > 0.16 μm), while two had >0.50 DC changes (H/V astigmatism > 0.32 μm). Although this study did not directly measure ocular aberrations, it has been shown that the near-work induced change in corneal aberrations was highly correlated with the change in ocular aberrations [14]. Thus, the small but significant corneal astigmatism induced after smartphone use might degrade the overall optical quality of the eyes, and also distance and near vision. When compared to previous studies (data were converted from Zernike coefficients to cylindrical error to aid in interpretation), the induced against-the-rule corneal astigmatism after smartphone use while walking appears to be higher than that after reading (~0.04 DC to 0.09 DC [13-15]) or using a computer (~0.03 DC [15]), but less than that after using a microscope (~0.21 DC [10]). Although the average astigmatic change was relatively small, it is possible that the experimental protocol may have led to an underestimation of optical aftereffects. It is worth noting that corneal aberration was measured after the near heterophoria assessment, i.e., the refractive measurement was not performed immediately after the smartphone use. The induced against-the-rule astigmatism could have decayed during the heterophoria assessment because participants were required to look straight ahead at the MIM chart, which may have led to the eyelid pressure exerted onto the cornea to have been reduced. The decay in optical aftereffects may also explain why the change in corneal astigmatism in the sitting position was not statistically significant, even though using a smartphone while sitting also involved a downward gaze.

Prolonged or intensive near work can also impose stress on the oculomotor system. After 30 minutes of smartphone use, the change in near heterophoria displayed relatively less exo- or more eso-deviation following walking than sitting, suggesting that the two experimental conditions imposed different stresses on the eyes. However, comparison of near heterophoria between baseline and post-smartphone use, showed there was no significant difference for either sitting or walking positions. Indeed, the effects of near work on binocular vision are inconsistent between studies. Whilst some studies revealed an esophoric shift following intensive near-work [19-21], others either showed an exophoric shift [18, 42, 43] or no significant change in heterophoria [44]. The discrepancies between studies could arise from the differences in their methodologies, including the near-work duration (from 20 to 90 mins), subject recruitment criteria (from children to adults), methods of vergence assessment, working distance (6.5 cm to 33 cm), and difficulty of the near task (reading, watching cartoon, visual search, and using virtual reality). This study indicated a difference in vergence adaptation between using smartphones in the walking and sitting conditions, although the change in near heterophoria did not reach clinical significance (limit of agreement for the modified Thorington test: 2.3Δ) [37]. Further studies are needed to better understand whether and how the direction of vergence adaptation relates to the oculomotor system.

This study allowed participants to use the smartphone freely, without restriction on their posture and viewing distance, to simulate a natural viewing condition. The change in corneal astigmatism and near heterophoria reported in this study should help better understand the visual disturbance suffered by smartphone users and the potential hazards for using the smartphone while walking. However, because this study did not control the viewing conditions and measure head and eye positions, the reasons behind the changes in corneal astigmatism and heterophoria are not conclusive. The coordination of the head and eye movement during the smartphone use (e.g., whether the user moved the head instead of the eye to stabilize the gaze) could affect the dynamic of eyelid pressure exerted on the cornea and the stress acting on the fusional vergence system. While it is not the primary purpose of this study to investigate the underlying causes of digital eye strain, it is worthwhile for further studies to be performed on how working distances, gaze direction, walking gait, and dynamic visual environment impose stress on the eyes.

To conclude, smartphone use while walking induced against-the-rule corneal astigmatism (i.e., a less negative corneal H/V astigmatism) and shifted the near heterophoria to be less exophoric when compared with the sitting condition. These significant optical and binocular vision changes–although small in magnitude–were observed in our young participants with normal vision. It would be important to investigate whether patients with binocular vision and accommodative anomalies would suffer from similar or even more effects.

Data file.

The study raw data.

(XLSX)

Click here for additional data file.

17 Jun 2020

PONE-D-20-16428

Smartphone Use while Walking Induced Optical and Vergence Aftereffects

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Reviewer #1: Thank you for asking me to review this concise and easy to read manuscript. I enjoyed reading it.

Title – I don’t think that this reflects the content of the manuscript. The vergence aftereffects were not statistically significant. You haven’t mentioned that your manuscript looks at the difference between walking and sitting while using the phone.

Abstract (conclusion): Final sentence “To ensure pedestrian safety….while walking”. This does not reflect the content of your manuscript, so I think it should be removed.

Introduction, page 3, lines 70-71. “Indeed, research has revealed…..related to visual quality”. These references refer to people with visual impairment, and is a different issue altogether from the content of the rest of the paragraph (and indeed, the manuscript). If you include these references then I think you should explain what visual quality parameters cause the problem and explain how it relates to the content of the manuscript. Otherwise, I think the sentence (and references) should be removed.

Experimental protocols (page 7), 2nd paragraph. “At each visit, the experiment began with…” The word “with” needs to be included.

Experimental protocols (page 7), 2nd paragraph. Three minutes dark adaptation – it’s not clear why did you did this. Was the experiment conducted in the dark? If someone is reading from a display with the luminance at maximum level, then they would not be dark-adapted anyway. Is 3-minutes long enough to dark adapt someone – probably not? Maybe you need to say that participants were seated in a darkened room for 3 minutes – and then explain why.

Results, page 10. “J0” and “J45”. I can guess what you mean by this, but I think it would be better to explain it to the reader rather than assume that they understand.

Discussion, page 14, last sentence of paragraph 1. “The patterns of near heterophoria change were also significantly different….” On the previous page you said that they were not statistically significant but “tended to show more exo-deviation”. I think you should reword this sentence in the discussion because you cannot say that the heterophoria change was significantly different.

Discussion, page 14, paragraph 2, 1st line. “…no matter smartphone usage…”. The sentence doesn’t make sense. Have some words been omitted?

Discussion, page 14, 15, 16. You discuss the change in downward gaze angle can alter the corneal curvature and cause astigmatism, and on page 16 (2nd paragraph) you mention “working distances, gaze direction, walking gait and dynamic visual environment” as possible stressors for the eyes. However, there is no mention of neck and head angle. I know that you didn’t measure this in this study, but it might have affected your results. For example, some people hold their phone below eye level and look downwards (and this could set up the lid-effects and astigmatism). Other people don’t move their eyes downward (i.e. the eyes are in a straight-ahead gaze position) but they bend/extend their head and neck forward to view the phone in their hands. This will have a different effect on the eye/lid dynamics. I think that you should mention this issue in the discussion.

Discussion, page 14, paragraph 2. You have cited other studies that have shown induced astigmatic changes with reading and microscopy. How does the magnitude of the changes you observed compare with the magnitude of changes reported in the other studies?

Reviewer #2: Thank you for the opportunity to review this paper. Although the writing is in standard English, the logic throughout the manuscript is unclear. With the following suggestions, the manuscript may be transformed into a useful addition to the literature.

Abstract:

Authors should consider the repeatability of heterophoria measurements. There are many papers and vergence after effect measurements in determining if the statistically significant finding for the vergence after effect has any real-life or clinical significance.

Introduction:

Argument in paragraph 2 of the introduction that mobility-related accidents are closely to related to visual quality is not well argued. Authors should consider the effects of divided attention and the smartphone will occupy the central visual field so the user is relying on more peripheral vision to navigate the environment. The authors could look to data on simulated and real central and visual impairment to understand the varied effects of location of visual field defects or scotomas have on mobility performance. There is a large literature on this. Visual stress is likely to be the least important factor when it comes to mobility problems and most patients who experience visual stress will avoid the activity unless it is absolutely necessary (e.g. work and study) rather than video streaming, playing games etc. Although the authors have raised issues with smartphone use, the argument is not logical. Visual stress also has more than one meaning in the vision science literature so this term should be defined within the manuscript.

The term “optical and vergence aftereffects” is not commonly used. It might be that the authors are thinking of short-term adaptation of the fusional vergence systems. The authors should review and include some of that literature in here and revise the language used. The authors should also clearly state the hypothesis, expected findings, in lieu of current understanding of fusional vergence adaptation and how it may be affected by posture and whether they are walking or static.

Methods and Rationale for the study design:

The authors need to provide an explanation of the refractive elements of the eye and their relative contribution to final refractive outcome and explain why the focus is only on the corneal refractive component, and then in the discussion explain what this means for interpretation of the study.

The authors need to explain much more clearly, using equations, the relationship between the magnitude of corneal astigmatism as measured using Zernike polynomials and in Dioptres. It is unclear what the clinical significance of the findings are. It is unclear whether Figures 1D and E are the same data depicted in two different units, or if post-condition refraction was conducted. What would the significance of a corneal shift in astigmatism be without an understanding of how the rest of the ocular elements are changed. For example, the act of convergence may potentially change the relative location of the refractive elements within the eye.

Results:

I found the results difficult to follow and could not determine whether Bonferroni correction was applied correctly. The authors should present all results clearly in a table with the multiple comparisons clearly shown. Non-significant findings after Bonferroni correction should be considered non-significant.

Discussion:

This should be revised after considering the additional literature that the authors will have included in the Introduction.

**********

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Reviewer #1: No

Reviewer #2: No

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13 Jul 2020

Reviewer #1:

Thank you for asking me to review this concise and easy to read manuscript. I enjoyed reading it.

Title – I don’t think that this reflects the content of the manuscript. The vergence aftereffects were not statistically significant. You haven’t mentioned that your manuscript looks at the difference between walking and sitting while using the phone.

Ans: Thank you for the comment. The title has been changed to “Changes in Corneal Astigmatism and Near Heterophoria after Smartphone Use while Walking and Sitting”. The short title has also been rephrased to “Optical and Heterophoria Effects after Smartphone Use”.

Abstract (conclusion): Final sentence “To ensure pedestrian safety….while walking”. This does not reflect the content of your manuscript, so I think it should be removed.

Ans: We agree with the reviewer's comment, the sentence has been removed.

Introduction, page 3, lines 70-71. “Indeed, research has revealed…..related to visual quality”. These references refer to people with visual impairment, and is a different issue altogether from the content of the rest of the paragraph (and indeed, the manuscript). If you include these references then I think you should explain what visual quality parameters cause the problem and explain how it relates to the content of the manuscript. Otherwise, I think the sentence (and references) should be removed.

Ans: By considering both reviewers’ comments, we agree that this sentence is irrelevant to the current content of the manuscript and it has been removed.

Experimental protocols (page 7), 2nd paragraph. “At each visit, the experiment began with…” The word “with” needs to be included.

Ans: Thanks. The word “with” is included (P7, L160).

Experimental protocols (page 7), 2nd paragraph. Three minutes dark adaptation – it’s not clear why did you did this. Was the experiment conducted in the dark? If someone is reading from a display with the luminance at maximum level, then they would not be dark-adapted anyway. Is 3-minutes long enough to dark adapt someone – probably not? Maybe you need to say that participants were seated in a darkened room for 3 minutes – and then explain why.

Ans: Sorry for the confusion and thanks for the suggestion. The purpose of “dark adaptation” was to dissipate any transient changes in accommodation and vergence before starting the measurements. We have rewritten the sentence and added relevant references (P7, L158-160).

Results, page 10. “J0” and “J45”. I can guess what you mean by this, but I think it would be better to explain it to the reader rather than assume that they understand.

Ans: Thanks for the comment. We’ve added equations to show the conversion from Zernike coefficients to dioptres and explain J0 and J45 in the Method section (P9, L199-207).

Discussion, page 14, last sentence of paragraph 1. “The patterns of near heterophoria change were also significantly different….” On the previous page you said that they were not statistically significant but “tended to show more exo-deviation”. I think you should reword this sentence in the discussion because you cannot say that the heterophoria change was significantly different.

Ans: We apologize for the mistake. We’ve revised the sentence to emphasize only this trend (P16, L317-318).

Discussion, page 14, paragraph 2, 1st line. “…no matter smartphone usage…”. The sentence doesn’t make sense. Have some words been omitted?

Ans: Thanks for pointing this out, we believe that the sentence is inappropriate and have deleted it.

Discussion, page 14, 15, 16. You discuss the change in downward gaze angle can alter the corneal curvature and cause astigmatism, and on page 16 (2nd paragraph) you mention “working distances, gaze direction, walking gait and dynamic visual environment” as possible stressors for the eyes. However, there is no mention of neck and head angle. I know that you didn’t measure this in this study, but it might have affected your results. For example, some people hold their phone below eye level and look downwards (and this could set up the lid-effects and astigmatism). Other people don’t move their eyes downward (i.e. the eyes are in a straight-ahead gaze position) but they bend/extend their head and neck forward to view the phone in their hands. This will have a different effect on the eye/lid dynamics. I think that you should mention this issue in the discussion.

Ans: Thanks for the suggestions. We agree with the reviewer that head and eye movements during the smartphone use might also affect our results. We’ve included this potential factor in the Discussion (P18-19, L384-389).

Discussion, page 14, paragraph 2. You have cited other studies that have shown induced astigmatic changes with reading and microscopy. How does the magnitude of the changes you observed compare with the magnitude of changes reported in the other studies?

Ans: We’ve added a sentence to compare the magnitude of change in corneal aberration between our study and other studies involving near works (P17, L344-348).

Reviewer #2:

Thank you for the opportunity to review this paper. Although the writing is in standard English, the logic throughout the manuscript is unclear. With the following suggestions, the manuscript may be transformed into a useful addition to the literature.

Abstract:

Authors should consider the repeatability of heterophoria measurements. There are many papers and vergence after effect measurements in determining if the statistically significant finding for the vergence after effect has any real-life or clinical significance.

Ans: Thanks for your comment. We’ve added a sentence in the Discussion to alert the readers that while the difference in vergence adaptation between walking and sitting was statistically significant, it did not reach clinical significance (P18 L374-376).

Introduction:

Argument in paragraph 2 of the introduction that mobility-related accidents are closely to related to visual quality is not well argued. Authors should consider the effects of divided attention and the smartphone will occupy the central visual field so the user is relying on more peripheral vision to navigate the environment. The authors could look to data on simulated and real central and visual impairment to understand the varied effects of location of visual field defects or scotomas have on mobility performance. There is a large literature on this. Visual stress is likely to be the least important factor when it comes to mobility problems and most patients who experience visual stress will avoid the activity unless it is absolutely necessary (e.g. work and study) rather than video streaming, playing games etc. Although the authors have raised issues with smartphone use, the argument is not logical. Visual stress also has more than one meaning in the vision science literature so this term should be defined within the manuscript.

Ans: Thanks for your comment. We agree with the reviewer that visual stress is not an essential factor in mobility compared to other factors, such as visual attention, scotomas, and visual field deficits. By considering both reviewers’ comments, we have removed the sentence “Indeed, research has revealed…..related to visual quality” (P3, L72).

The term “optical and vergence aftereffects” is not commonly used. It might be that the authors are thinking of short-term adaptation of the fusional vergence systems. The authors should review and include some of that literature in here and revise the language used.

Ans: Thanks for pointing this out. We’ve revised the terminology and changed “vergence aftereffect” to “vergence adaptation” throughout the manuscript.

The authors should also clearly state the hypothesis, expected findings, in lieu of current understanding of fusional vergence adaptation and how it may be affected by posture and whether they are walking or static.

Ans: Thank you. We’ve added a paragraph in the Introduction to state the rationale and hypothesis of this study (P4-5, L85-106).

Methods and Rationale for the study design:

The authors need to provide an explanation of the refractive elements of the eye and their relative contribution to final refractive outcome and explain why the focus is only on the corneal refractive component, and then in the discussion explain what this means for interpretation of the study.

Ans: Thanks for the comment. We’ve added an explanation of why we focused on corneal aberration and how it might contribute to the variation of the overall optics of the eye in the Method section (P9, L193-197). We’ve also discussed the potential visual consequence of the aberration change in the Discussion (P17, L339-344).

The authors need to explain much more clearly, using equations, the relationship between the magnitude of corneal astigmatism as measured using Zernike polynomials and in Dioptres.

Ans: Thanks. We’ve added the equations for the conversion from Zernike coefficients to dioptres in the Method (P9, L199-207).

It is unclear what the clinical significance of the findings are.

Ans: We’ve added a sentence to discuss the potential visual consequence of the aberration change in the Discussion (P17, L342-344).

It is unclear whether Figures 1D and E are the same data depicted in two different units, or if post-condition refraction was conducted.

Ans: Figure 1D and E represent oblique astigmatism with the same unit as the H/V astigmatism (B & C). To make it clearer, we’ve revised the figure legend (P13, L256-260). Sorry for the confusion.

What would the significance of a corneal shift in astigmatism be without an understanding of how the rest of the ocular elements are changed. For example, the act of convergence may potentially change the relative location of the refractive elements within the eye.

Ans: Due to the restriction of our study design, we could only selectively measure part of the ocular biometric changes. However, we agree with the reviewer that other potential factors could contribute to the variation of the corneal shape and aberrations. We’ve included these factors in the discussion (P16, L331-334), as well as rationale for why we focused on corneal aberration (P9, L193-197).

Results:

I found the results difficult to follow and could not determine whether Bonferroni correction was applied correctly. The authors should present all results clearly in a table with the multiple comparisons clearly shown. Non-significant findings after Bonferroni correction should be considered non-significant.

Ans: Sorry for the confusion. We have added a table to summarize the statistics (P12, L236-242).

Discussion:

This should be revised after considering the additional literature that the authors will have included in the Introduction.

Ans: The Discussion section is revised. Thanks.

Submitted filename: Response to reviwers comments.docx

Click here for additional data file.

23 Oct 2020

PONE-D-20-16428R1

Changes in corneal astigmatism and near heterophoria after smartphone use while walking and sitting

PLOS ONE

Dear Dr. Leung,

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Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: I Don't Know

Reviewer #2: Yes

**********

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The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

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PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Well done. You've done a great job revising this manuscript. I especially like the inclusion of Table 2.

Reviewer #2: Thank you for the revision. Only one additional query has come up. When watching the movie on the smart phone, were they watching a movie in a language that required them to read the subtitles? In other words, were the subtitles an essential part of the experimental condition?

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

31 Oct 2020

Reviewer #1:

Well done. You've done a great job revising this manuscript. I especially like the inclusion of Table 2.

Thank you very much for reviewing this manuscript and providing valuable comments.

Reviewer #2:

Thank you for the revision. Only one additional query has come up. When watching the movie on the smart phone, were they watching a movie in a language that required them to read the subtitles? In other words, were the subtitles an essential part of the experimental condition?

Thank you very much! It’s an excellent question. Sorry that we have missed it in the previous version. We played a Korean variety show called “Running Man”, a popular foreign TV program in Hong Kong, for 30 minutes with Chinese subtitle (subtitle’s size: ~ 3mm). None of the participants knew Korean, and reading the subtitle was necessary. This information has been added in the revised version (P7, L159-161).

Submitted filename: Response to reviwers comments.docx

Click here for additional data file.

16 Nov 2020

Changes in corneal astigmatism and near heterophoria after smartphone use while walking and sitting

PONE-D-20-16428R2

Dear Dr. Leung,

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Blanka Golebiowski, PhD BOptom

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

19 Nov 2020

PONE-D-20-16428R2

Changes in corneal astigmatism and near heterophoria after smartphone use while walking and sitting

Dear Dr. Leung:

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