Thirty-five healthy volunteers who had better than 16/20 uncorrected visual acuity with above 20/20 best-corrected visual acuity were recruited. The subjects had no ophthalmologic diseases, including strabismus, amblyopia, corneal or retinal disease, or a history of ocular surgery, except for refractive surgery. The number of subjects was calculated using G-power version 3.1 (Heinrich Heine university, Dusseldorf, Germany) and considered a drop-out rate of 20%. Twelve subjects with exophoric deviation > 10 prism diopters (PD) and/or esophoric deviation > 5 PD were excluded. Informed consent was obtained from all 23 volunteers who were eligible and ultimately enrolled in this study. Ethics committee approval was obtained from the Chonnam National University Hospital Institutional Review Board (Gwangju, Korea). The study protocol adhered to the guidelines of the Declaration of Helsinki.
Display
The Oculus Rift VR device (Oculus VR, LLC., Irvine, California, USA) was used in this study. The device comprised a lightweight (0.44 kg) headset that completely covered the field of view. The headset included separate displays for each eye, each with 960 × 1080 resolution, yielding a 100-degree-horizontal field of view. A fixed-degree convex lens was located in front of each display rendered display content at optical infinity. Inter-pupillary distance was adjusted via a user-enabled key that was located on the right side of the VR device.
Participants used the Oculus Rift device while seated on a freely rotating chair. They were asked to perform 30 min of game play (Minecraft, Mojang AB, Sweden) in two different modes (immersive and non-immersive). There was a 1-week interval between playing in immersive mode and non-immersive mode. In the immersive mode, the stereo head-tracking head-mounted display presentation brought the player inside the 360-degree virtual reality environment which allowed the user to feel as if they were physically present in the game. The viewpoint moves in accordance with the player’s head movements. In the non-immersive mode, the player is placed in a static environment (e.g., a living room) while watching the VR environment on a desktop screen that was approximately 2 m away (a desktop view). The players could look around the room; however, the area of game-play was fixed on a virtual screen in front of the player (Additional file 1).
Measurements of accommodation
Refraction and accommodation were measured using a binocular open-field refractor (Auto Ref/Keratometer WAM-5500, Grand Seiko Co Ltd, Hiroshima, Japan). The spherical equivalent (sphere + 1/2 of cylinder) was used for calculation. For static measurement, the accommodative amplitude was calculated by subtracting the refractions obtained under monocular condition while viewing a 1 cm × 1 cm E-shape target at 33 cm from those obtained from viewing the target at 5 m in the same manner.
Software verified by the manufacturer was installed on a computer to allow dynamic mode function. To initiate measurements, the instrument was aligned with the pupil of each eye, and the joystick button was pushed and then released once; the instrument then commenced recording dynamic measurements at approximately 5 samples/s.The observer ensured that the instrument remained carefully aligned with the subject’s right eye while undergoing dynamic measurements by observing the alignment target imaged within the pupillary center in the LCD monitor for the entire duration of testing. The instrument wrote the data to a spreadsheet file (Excel, Microsoft Corporation, Redmond, WA, USA) that recorded the time of measurement, eye measured, spherical equivalent refraction, and pupil diameter approximately every 0.2 s and converted it to a sine graph form [16]. The velocity of accommodation, mean accommodative lag, and dynamic accommodative response was investigated to measure dynamic accommodation.
The velocity of accommodation was obtained by calculating the difference between the maximum and minimum refraction divided by the time taken. Mean accommodative lag was calculated by averaging the value of the participant’s actual refraction that differed from the target refraction. The dynamic accommodative response was calculated according to the dispersion between actual refraction and target refraction. A higher correlation coefficient was associated with better dynamic accommodative response (Fig. 1).
Other visual parameters
Monocular near point of accommodation (NPA) was obtained using Donder’s push-up method. A 20/30 single letter on a fixation stick, approximately 50 cm from the subject, served as the target and was moved gradually closer to the subject at a rate of approximately 5.0 cm/s until the subject noticed the target starting to blur.
The near point of convergence (NPC) was also obtained. The fixation target, the starting point of examination, and the moving velocity of the fixation target were the same as those previously described for the NPA measurement. The first point at which the corneal reflex of the subjects began to extend outward was considered to be the endpoint. Near stereopsis was measured using a near stereopsis vision test (Stereo Fly SO-001 test; Stereo Optical Co., Chicago, IL, USA). The test stereogram was held 40 cm from the subject during the test. Threshold stereopsis level was recorded in arc seconds.
Ocular dominance was determined by the hole-in-the-card test, in which the subject was asked to hold a card with a hole at arm’s length and focus on an objective 3 m away with both eyes. The examiner then alternately occluded the eyes to determine which eye was viewing the object through the hole, and the eye concluded to be viewing the object was determined to be the dominant eye.
The presence and magnitude of far (5 m) and near (33 cm) phoria were verified using the cover test and alternating cover test with prism. A standard set of loose plastic prisms was used for all measurements. The individual prisms increased in power from 1 PD to 10 PD in 1-PD increments, and from 10 to 20 PD in 2-PD increments. All measurements were repeated 3 times for each tested eye, with results reported as the mean value.
All measurements were performed before and immediately after playing the VR game in the order listed above. If visual parameters were changed, it was measured repeatedly every 15 min until the initial value was obtained again. The criteria for re-examination were > 2-cm changes in NPA and NPC, over 20 seconds of arc change of stereopsis, and over 0.5 D change of refraction. Ocular phoric deviation was evaluated by the same pediatric ophthalmologist (H.H.). The other visual parameters were examined by a single examiner (H.J.Y.).
Evaluation of subjective symptoms
Thirteen symptoms were included in the questionnaire. The questionnaire was based on a computer vision syndrome questionnaire previously described by Seguí del M et al. [17]. The symptom sensation questionnaire contained six identical analogue scales (0 = none, 6 = too severe to tolerate) through which the subject recorded the magnitude of each of the symptoms compared with baseline. After playing two modes of the VR game, the subjects completed the questionnaire.
Statistical analysis
Statistical analysis was performed using SPSS version 18.0 (IBM Corporation, Armonk, NY, USA) for Windows (Microsoft Corporation, Redmond, WA, USA). The normal distribution for all variables was assessed using the Kolmogorov-Smirnov test. All variables were not normally distributed. Data are presented as the median (interquartile range). A Wilcoxon signed rank test was used to compare changes in variables before and after performing VR. Differences in subjective symptoms according to the contents were also compared using the Wilcoxon signed rank test. Spearman’s rho correlation test between each of the visual parameters was used for correlation analysis. The variables for a single eye, including NPA and accommodative parameters, were solely correlated with the corresponding eye. For all tests, statistical significance was determined to be p < 0.05. with differences corrected by the Benjamini-Hochberg procedure using false discovery rates of 0.25.