Abstract
Purpose:
This study aimed to investigate the effect of virtual reality (VR) technology in children after surgery for concomitant strabismus.
Methods:
A total of 200 children with concomitant exotropia or concomitant esotropia were randomly divided into a training group and a control group according to the single even number random method (100 cases in each group). Patients in the training group received VR intervention training within 1 week after surgery. Patients in the control group did not receive any training.
Results:
Six months after the surgery, the orthophoria (the far or near strabismus degree was ≤8D) rate was significantly higher in the training group than in the control group (P = 0.001), while the eye position regression rate (compared to the strabismus degree within 1 week after the surgery, the amount of regression >10D) was significantly lower in the training group than in the control group (P = 0.001). Six months after the surgery, the number of children with simultaneous vision and remote stereovision was significantly higher in the training group than in the control group (P = 0.017 and 0.002, respectively). The differences in the number of patients with peripheral stereopsis, macular stereopsis, and stereopsis in macular fovea centralis at 1, 3, and 6 months after the surgery between the training and the control groups were not statistically significant (P = 0.916, 0.274, and 0.302, respectively).
Conclusion:
The intervention of VR technology after strabismus correction effectively improved children’s visual function and maintained their eye position.
Keywords: Binocular vision, concomitant strabismus, eye position, virtual reality technology
“Strabismus” is a condition in which the two eyes cannot look at the target simultaneously. While one eye will be able to focus on the target, the other will deviate from the item.[1,2] Concomitant strabismus is a condition in which the eyeballs have no movement disorder. In this instance, the strabismus degree will be the same when the left or the right eye is watching, respectively, and the strabismus degree will be the same when both eyes move in any direction. The pathogenesis of the disease is complex and remains unknown. It is generally believed to be related to heredity, refractive coordination, and an eye muscle imbalance. At present, surgery remains the main treatment for improving the appearance and binocular visual function. However, some patients are prone to eye position reversion after surgery, resulting in disease recurrence. This affects the normal development of children’s visual function and they may even require reoperation.[3]
Virtual reality (VR) technology has rapidly developed in recent years and includes knowledge related to visual neurology, binocular vision, and applied optics. In addition, smart glasses and “head-mounted displays” (HMDs) have become easier to operate; accordingly, VR technology has become a popular and difficult topic in the diagnosis and treatment of ocular visual diseases in recent years.[4-7] In the past, VR technology had achieved good results in the treatment of patients with amblyopia. However, the application value of VR technology in concomitant strabismus remains under discussion. Accordingly, the research team conducted a comparative study on children with concomitant strabismus who were treated in the authors’ hospital to explore the value of VR technology in the postoperative adjuvant treatment of strabismus. The details are reported as follows.
Methods
General information
From January 2019 to June 2021, 200 children with concomitant exotropia or concomitant esotropia undergoing surgery in the authors’ hospital were enrolled in this study. The inclusion criteria were as follows: (1) children aged 4–16 years with normal intellectual development; (2) children with concomitant exotropia or esotropia who could communicate well with the examiner and cooperate in the examination and treatment; and (3) children’s family members voluntarily accepted treatment. The exclusion criteria were as follows: (1) children with ocular organic diseases, such as keratopathy, cataract, glaucoma, uveitis, ocular trauma, and fundus disease, or children with a previous history of eye surgery; (2) children with strabismus of <15D; (3) children who were unable to cooperate in the examination and treatment or were still unable to understand the process after completing a binocular vision examination; and (4) children who exhibited any discomfort, were unable to complete the test, or who requested to withdraw from the test during the study. This study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Capital Institute of Pediatrics Affiliated Children’s Hospital. Written informed consent was obtained from the participants’ legal guardian to participate in the study.
Clinical Methods
Inspection methods
The patients in both groups underwent routine examinations after admission, including visual acuity, anterior segment, refractive medium, fundus examination, eye position, and eye movement. All children underwent retinoscopy under ciliary paralysis to correct ametropia. All children with esotropia underwent correction using glasses able to address the full scope of hyperopia.
Deviation examination was conducted using the following:
-
(1)
An LG2342p polarized three-dimensional (3D) display inspection device with a refresh rate of 120 Hz and resolution of 1920 × 1080 using the Windows XP system, and a personal computer host; the visual perception inspection and evaluation system was formulated with reference to the relevant technologies of the National Engineering Research Center for Healthcare Devices. The items of visual perception inspection and evaluation system are shown in Fig. 1. During examination, the children were in the sitting position and wore polarized glasses for split vision. Both eyes were at the same height as the central point of the display at a distance of 80 cm, and feedback was carried out by operating a computer mouse.
-
(2)
The parameter settings were as follows: the stimulation angle was 38° × 18°, the gray background was 44 cd/m2, and the size was 51 cm × 29 cm.
-
(3)
The following examination methods were conducted: The participants looked at the stimulus image while wearing polarized glasses. During polarized glasses split vision, the child’s right eye looked at the circle and the left eye looked at the cross. The participant placed the cross into the circle. The examination was performed under the participants’ best-corrected visual acuity, the deviation was calculated in pixels, and a deviation of 53 pixels was equivalent to 1°. Each patient’s examination was repeated three times, and the mean was regarded as the final result.
Figure 1.
(a) The child wore polarized glasses. His (her) right eye looked at the circle and left eye looked at the cross, and the subject put the cross into the circle alone. The deviation was calculated in pixels, and a deviation of 53 pixels was equivalent to 1°. (b) Check for monocular inhibition. If the left eye is inhibited, the child can only see squares 2 and 3. If the right eye is inhibited, the child can only see squares 1 and 4. If not, the child can see four squares. The squares on both sides represent the nasal and temporal sides of the left or right eye. (c) Check for rough stereopsis. For example, if asked to indicate if wave 2 (number 2 in the circle) is convex or concave, the child chooses the corresponding button according to what he (she) sees. (d) Check for dynamic stereopsis. The dots in the background change dynamically. There is a protruding “E” vision mark in the background. The child needs to point out the direction of the E vision mark
Therapeutic methods
Children underwent strabismus correction under general anesthesia. Children in the training group received VR intervention training within 1 week of the procedure. Children in the control group did not receive any training. The intervention plan comprised obtaining the detailed parameters of the children’s binocular imbalance according to the perceptual eye position examination. First, in the hospital, two training sessions were conducted and parents were instructed on how to participate in the treatment. Then, training was carried out for 15–20 min twice daily at home for 3 months. The training was meant to be assisted by parents to ensure credibility of the results. All children were followed up at 1, 3, and 6 months after training. The training refers to the push–pull model personalized training system, based on VR technology provided by the National Engineering Research Center for Healthcare Devices. The training plan involved children sitting upright in front of a computer and wearing smart glasses or HMD equipment that comprised red and blue lenses on the left and right, respectively. Level III stereopsis training involved 10-min sessions each time, a 5° image, with alternating blinking to enable the eyes to see the stimulation images at different times. The blinking frequency was set to five times per second. Then, simultaneous blinking training was conducted. The frequency, time, and images were the same as those that were used for the alternating blinking training. Level II fusion training comprised convergence, and separate training was carried out for 10 min each time, respectively. Level I simultaneous vision function training involved using a stereopsis blinking scheme.
Observation indexes
The eye position correction rate, reversion rate, three-level visual function, near stereopsis, and perceptual eye position of all subjects at 1, 3, and 6 months after the procedure were statistically analyzed as follows: (1) A single eye was covered for 1 h to fully expose the strabismus angle. Then, the degree of the strabismus was tested by prism neutralization at distances of 33 cm and 6 m. The average strabismus degree of far and near vision was used to compare the eye position of patients. The eye position judgment criteria were as follows: in the case of obvious under-correction or over-correction, the far or near strabismus degree was ≥15D. Mild under-correction or over-correction reflected a far/near strabismus degree of >8D. In the case of normotopia (including hidden deviation and small-degree deviation), the far or near strabismus degree was ≤8D. The eye position reversion judgment criteria were as follows: when compared to the strabismus degree within 1 week after the surgery, the amount of reversion >10 ∆ was regarded as indicating eye position reversion. (2) The near stereovision function was examined using a Titmus stereogram. Simultaneous vision, visual fusion, and remote stereovision function were examined using a synoptophore. Under natural light, the visual axis was perpendicular to the Titmus stereoscopic image; the distance from the subject’s eye was 30 cm, and the subjects wore polarized 3D glasses and corrective glasses to measure the near stereopsis function. The judgment standard was that a value of >800 indicated no stereopsis, 400–800 was indicative of peripheral stereopsis, 80–200 indicated macular stereopsis, and ≤60 was indicative of stereopsis in macular fovea centralis. In the synoptophore examination, a Haag-Streit 2001 machine was used. Level I simultaneous vision function was measured using the lion-in-a-cage image, level II visual fusion function using the cat/butterfly image, and level III stereopsis function using the colored fish image.
Statistical analysis
Data were processed using Statistical Package for the Social Sciences (SPSS) statistics 26.0 software program. Normally distributed measurement data were expressed as mean ± standard deviation (x¯ ± SD) and compared between the two groups using t-tests. Non-normally distributed measurement data were expressed as median (M) (1/4, 3/4) and compared between the two groups using Mann–Whitney U tests. Count data were expressed as rates and compared between the two groups using the Chi-squared (χ2) and exact probability tests. A P value < 0.05 was considered statistically significant.
Results
Comparison of general data between the two groups of children
There were no significant differences in gender, age, and diopter between the two groups (P = 0.120, 0.177, and 0.876, respectively), so also was the strabismus composition (exotropia/esotropia) between the two groups (84%/16% in the training group and 85%/15% in the control group, P = 0.845). There were no significant differences in the absolute value of preoperative strabismus degree and perceptual eye position (pixels) between the two groups (P = 0.351 and 0.335, respectively) [see Table 1].
Table 1.
Comparison of general data between the two groups of children (n [%], x¯ ± SD)
Training group (n=100) | Control group (n=100) | t/χ2 | P | |
---|---|---|---|---|
Gender (male/female) | 54/46 | 43/57 | 2.422 | 0.120 |
Age (years) | 6.28±2.18 | 6.74±2.61 | 1.354 | 0.177 |
Hyperopia/myopia* | 72/28 | 71/29 | 0.025 | 0.876 |
Mild | 55/24 | 61/23 | ||
Moderate | 15/4 | 7/6 | ||
Severe | 2/0 | 3/0 | ||
Strabismus composition (exotropia/esotropia) | 84/16 | 85/15 | 0.038 | 0.845 |
Absolute value of preoperative strabismus (∆) | 33.40±12.60 | 35.35±16.68 | 0.935 | 0.351 |
Perceptual eye position (pixels) | 320.13±153.74 | 347.89±177.98 | 0.967 | 0.335 |
SD=standard deviation. *Myopia or hyperopia and their degree are evaluated in eyes with large absolute value of spherical equivalent after mydriasis
Comparison of eye position correction rate and reversion rate between the two groups
There were no significant differences in the correction and reversion rates of eye position between the training and control groups 1 and 3 months after the operation. Six months after the procedure, the correction rate of the eye position in the training group was significantly higher than in the control group (P = 0.001) and the reversion rate of eye position in the training group was significantly lower than in the control group (P = 0.001) [Table 2].
Table 2.
Comparison of eye position correction rate and reversion rate between the two groups of children (n [%])
Group | Correction rate (%) | Reversion rate of eye position (%) | ||||
---|---|---|---|---|---|---|
|
|
|||||
1 month after operation | 3 months after operation | 6 months after operation | 1 month after operation | 3 months after operation | 6 months after operation | |
Training group | 97.00 | 93.00 | 94.00 | 0.00 | 4.00 | 5.00 |
Control group | 93.00 | 85.00 | 78.00 | 4.00 | 11.00 | 20.00 |
χ 2 | 1.684 | 3.269 | 10.631 | * | 3.532 | 10.286 |
P | 0.194 | 0.071 | 0.001 | 0.061 | 0.060 | 0.001 |
*Exact probability test
Comparison of visual function between the two groups of children
There were no significant differences in simultaneous vision, visual fusion, and remote stereopsis between the training and control groups 1 and 3 months after the procedure. Six months after the operation, the number of children with simultaneous vision and remote stereovision in the training group was significantly higher than those in the control group (P = 0.017 and 0.002, respectively). Although there was no significant difference in visual fusion between the two groups, the difference was close to the cutoff value (P = 0.053) [see Table 3].
Table 3.
Comparison of visual function between the two groups of children (n [%])
Group | Simultaneous vision | Visual fusion | Remote stereovision | ||||||
---|---|---|---|---|---|---|---|---|---|
|
|
|
|||||||
1 month after operation | 3 months after operation | 6 months after operation | 1 month after operation | 3 months after operation | 6 months after operation | 1 month after operation | 3 months after operation | 6 months after operation | |
Training group | 93.00 | 96.00 | 99.00 | 68.00 | 79.00 | 89.00 | 41.00 | 52.00 | 66.00 |
Control group | 86.00 | 91.00 | 92.00 | 66.00 | 75.00 | 79.00 | 28.00 | 41.00 | 44.00 |
χ 2 | 2.607 | 2.057 | * | 0.090 | 0.452 | 3.720 | 3.739 | 2.432 | 9.778 |
P | 0.106 | 0.152 | 0.017 | 0.764 | 0.502 | 0.054 | 0.053 | 0.119 | 0.002 |
*Exact probability test
Comparison of near stereovision acuity between the two groups of children
At 1, 3, and 6 months after the operation, there were no significant differences between the training and the control groups regarding stereopsis in macular fovea centralis, macular stereopsis, and peripheral stereopsis (P = 0.916, 0.274, and 0.302, respectively) [see Table 4].
Table 4.
Comparison of near stereovision acuity between the two groups of children (n [%])
Group | 1 month after operation | 3 months after operation | 6 months after operation | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
|
|
|
||||||||||
① | ② | ③ | ④ | ① | ② | ③ | ④ | ① | ② | ③ | ④ | |
Training group | 31.00 | 50.00 | 12.00 | 7.00 | 40.00 | 50.00 | 7.00 | 3.00 | 59.00 | 34.00 | 6.00 | 1.00 |
Control group | 34.00 | 50.00 | 11.00 | 5.00 | 44.00 | 39.00 | 14.00 | 3.00 | 47.00 | 40.00 | 11.00 | 2.00 |
χ 2 | 0.515 | 3.883 | 3.649 | |||||||||
P | 0.916 | 0.274 | 0.302 |
(1) Stereopsis in macular fovea centralis, (2) macular stereopsis, (3) peripheral stereopsis, and (4) no near stereovision acuity
Comparison of postoperative perceptual eye position between the two groups of children
There was no significant difference in perceptual eye position at 1, 3, and 6 months after the operation between the training and control groups (P = 0.841, 0.315, and 0.079, respectively) [see Table 5].
Table 5.
Comparison of postoperative perceptual eye position between the two groups of children (n [%])
Group | 1 month after operation | 3 months after operation | 6 months after operation |
---|---|---|---|
Training group | 56.00 (27.00, 113.50) | 29.00 (13.00, 52.00) | 19.00 (12.00, 42.00) |
Control group | 54.50 (25.50, 149.50) | 31.50 (13.50, 79.00) | 24.00 (13.00, 79.00) |
U | 3374.500 | 3823.500 | 3845.500 |
P | 0.841 | 0.315 | 0.079 |
Discussion
Binocular vision relies on the visual center processing the external 3D information obtained by both eyes. The most advanced binocular visual functions include remote stereovision and near stereovision. The latter is a stereoscopic perception jointly formed by regulation and convergence, while remote stereovision is a stereoscopic perception formed in static conditions. In normal physiological conditions, binocular vision is closely related to brain image fusion function and requires normal retina correspondence and simultaneous binocular vision. However, due to congenital or acquired factors, some children’s binocular visual axes are not parallel, that is, the condition of strabismus, which induces abnormal correspondence of the retina or inhibition of binocular visual information, resulting in the decline of children’s motor skills.[8,9] Concomitant strabismus is the most common type of this condition. The cause of the disease remains unclear. Clinically, surgery is often adopted to correct the eye position of children. However, depending on children’s treatment compliance, the operator’s experience, and other factors, children may experience eye position reversion, under-correction, or over-correction after surgery.[10] Eshaghi et al.[11] considered that the degree of postoperative visual function recovery was related to the type and time of preoperative strabismus, amblyopia, and postoperative eye position. Research conducted by Liu[12] revealed that when children were treated with visual training after correction, their stereovision function was significantly improved.
The results of this experiment revealed that 6 months after surgery, the reversion rate of eye position in the training group was significantly lower than in the control group, while the correction rate was significantly higher, suggesting that postoperative VR intervention helped to improve the eye position of children. The reason for this may be that VR comprises the construction of a fully digital 3D virtual environment. What users see when using this technology is a fully constructed virtual scene, which makes their senses, such as touch, hearing, and vision, receive comprehensive stimulation under immersive conditions. The training is designed for children and attracts their attention, making it easy for them to engage and cooperate. VR technology presents significant advantages. For example, the technology provides for the creation of a broad imaginable space. Additionally, children can be immersed in a “real” virtual environment and interact with specific virtual scenes to fully mobilize their sensory functions; additionally, children can be immersed within a completely virtual environment that they can experience from a personal perspective, thereby experiencing a stronger sense of being in the scene.[13,14]
VR technology may play an important role in the diagnosis and treatment of various ophthalmic diseases.[15,16] Researchers are constantly developing training software to adapt to a range of diseases. VR technology can induce the neural plasticity of children with amblyopia using supporting software.[17] Accordingly, VR technology may have the same inducing effect on children with strabismus through targeted software training.
In clinical practice, the authors found that children’s visual function was still developing. The conceptual, interactive, and immersive properties of VR technology can positively impact children’s sense of visual balance and distance. Binocular vision comprises simultaneous vision, visual fusion, and stereovision. The normality of retina correspondence and simultaneous vision via both eyes is closely related to the mechanism of stereoscopic vision. Near stereovision includes stereopsis in macular fovea centralis, macular stereopsis, and peripheral stereopsis, which mainly participate in the regulation of dynamic stereopsis through pupil response, convergence, and accommodation. The results of this experiment revealed that 6 months after the surgery, the training group’s results were significantly better compared to the control group, in terms of the three-level function of binocular vision. Although there was no significant difference in near stereovision between the training and control groups at 1, 3, and 6 months after the operation, data of the training group were still better than those of the control group. After the surgery, the eye position was corrected and the binocular vision and brain required a process of readjustment. VR training can be applied in a more targeted and effective manner in this remodeling process, which will be conducive to the recovery of binocular visual function. Dai et al.[18] promoted the recovery of binocular visual function by conducting binocular visual training for children with intermittent exotropia after the operation, with results showing high safety.
Conclusion
The intervention of VR technology after the correction of concomitant strabismus can effectively improve binocular visual function, maintain eye position, and improve the cure rate after strabismus surgery.
Financial support and sponsorship
This study was supported by the Special Fund of the Pediatric Medical Coordinated Development Center of Beijing Hospitals Authority (No. XTYB201832).
Conflicts of interest
There are no conflicts of interest.
Acknowledgements
We would like to acknowledge the technical support of National Engineering Research Center for Healthcare Devices, Guangzhou, China, and express our gratitude to professor Ya-Qin Zhang of Capital Institute of Pediatrics, who provided statistical analysis support.
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