1 Introduction

Recent population-based studies among school children quote a higher prevalence of non-strabismic binocular vision anomalies [1-3]. Until and unless the signs manifest as either poor academic performance [4-7] or decompensate to strabismus these issues go unnoticed. Therefore, screening of binocular abnormalities is important among school children, to find and treat, if possible, any anomaly which may further lead to visual discomfort and disability. This demands further attention when it comes to children with hearing impairment and speech difficulties.

Compared to people with normal hearing and speech, deaf people are thought to view the world differently. The eyes are used for communication, and interpret sign language and facial expressions. Therefore, it is extra important to diagnose and treat visual defects. Visual defects among the deaf are more common which include refractive errors and anomalies of binocular vision [8, 9]. Vision screening is vital for children with developmental delay, speech and hearing impairment to detect and treat any visual discomfort that can impact their visual performance [8].

When screening children for binocular abnormalities, some of the tests usually require the participant to be able to understand and answer questions given by the examiner. In children with speech and hearing impairment this might be a problem, especially in screenings when most of the tests depend on subjective response. To the best of our knowledge, not many studies have investigated binocular vision anomalies in children with speech and hearing impairment due to the challenges discussed above. One study carried out on children with congenital hearing impairment from a similar ethnicity showed higher percentage of heterophoria and accommodation anomalies [10]. Nonetheless information on the age matched comparative group is not clear in this study.

Thus, the aim of this study was to estimate the near point of convergence (NPC) and near phoria measurements objectively in children who have hearing and speech impairment and to compare the results to typically developing children without any hearing/speech impairment (emmetropic Children). This study intended to understand the differences in these binocular vision impairments and propose guidelines for future screenings and studies.

2 Methodology

The study was approved by the institutional review board and ethics committee of Vision Research Foundation, Chennai, India and followed the guidelines of the Declaration of Helsinki. The informed consent from parents or guardians was obtained for all the Children who participated in this study by writing.

A total of 279 Children were selected for the study that included 93 participants with hearing and speech impairment, who were chosen from two schools for speech and hearing impairment in South India, and 186 age matched control Children were recruited through the school vision screening program carried out in one regular school during the same study period. The students chosen as controls had no hearing, speech or developmental abnormalities. Children with ametropia, visual acuity lower than 20/30 at distance (0.2 Log MAR or 6/9 Snellen equivalent), N6 near visual acuity, manifest strabismus, and ocular abnormalities other than non-strabismic binocular vision abnormalities [1, 11], were excluded from the study. For the binocular vision assessment, children who passed the initial vision screening and who were not wearing any refractive correction were considered. Children who were using a refractive correction and/or who failed the vision screening were referred for refractive correction and were not included in any of the groups. For a detailed description of the school eye health protocol, refer to Narayanan et al. [12].

Children with HI were instructed through sign language by their teacher and training session which related the procedures of screening in a group setting before screening began. None had cochlear implants. A sign language helper was always present throughout the process to clarify any doubts the children or examiner had with respect to interpreting the instructions.

For near phoria measurement, a prism cover test was used at 40 cm to neutralize the deviation in children with hearing impairment and modified Thorington method was used in the age matched controls. The reliability and comparability of these procedures is well established [13, 14]. Alternate prism cover test was done where the eye movement was observed until the eye showed no movement with increasing amounts of prism. The participants were instructed to focus on a 6/9 (reduced Snellen) row of vertical letters. The power of the prism was recorded as the magnitude of phoria.

For the modified Thorington test, a Maddox rod was placed in front of right eye, whilst the participant was directed to look at the muscle imbalance measure (MIM) card at 40 cm. The participants were instructed to show where the red line appeared, while looking at the light in the middle of the card.

For NPC measurement, an Astron International rule consisting of accommodative target with a linear row of letters of 6/9 reduced Snellen size was used [15]. The children were instructed to fixate on a single letter which is brought slowly closer to their nose at a speed of 1 cm/s. Once breaking of fusion is observed by the deviation of eyes objectively by the examiner, the distance between the target and the eye is measured through a ruler placed on the forehead and this was considered as the end point for break. The target then was taken back until the eyes restored alignment that provided the recovery point for NPC measurement. The test was repeated three times and an average of three measurements were taken as the break point. This procedure was preferred over using the conventional techniques for both simplicity of administration and measurement. As children with HI potentially can have issues regarding comprehension and providing subjective responses through sign language, a single examiner correlated the subjective response with the objective endpoints, the objective deviation of the eyes during testing for NPC, and the reversal of the eye movement with the prism cover test. This was consciously ensured throughout the study data collection.

The diagnostic criteria for non-strabismic binocular vision anomaly (NSBVA) of convergence insufficiency (CI) and cut-off for near phoria and NPC were set based on the BAND study [15, 16]. A diagnosis of CI was confirmed if the participant had both near phoria greater than or equal to 4Δ Exophoria and NPC greater than 6 cm [15, 16].

3 Results

The mean (± standard deviation) age of controls and children with hearing impairment are 10.7 ± 2.8 years and 10.7 ± 2.7 years respectively, the difference of which was not statistically significant (Independent t-test, p > 0.05).

The near Phoria and NPC showed a statistically significant difference between the controls and children with hearing impairment, with higher values in the HI group. Table 1 shows median values of binocular vision among the two groups.

The proportion of children with receded NPC, exophoria and CI in HI and control group were compared using the Z-Test (Table 2).

As the age range of children enrolled into this study belonged to the ages where visual development could influence the binocular vision parameters, we also carried out a sub-group analysis categorizing the age into two bins of 6–10 years and 11–15 years. Analysis of phoria and NPC within the two age bins did not show statistically significant difference within the groups (Mann-Whitney U test, p > 0.05). When these parameters were compared between the groups of controls and HI, a statistically significant difference continued to exist in both the age bins for phoria, and for the 6–10 years age bin for NPC (Mann Whitney U test, p < 0.05) (Table 3). Both phoria and NPC values continue to be receded across the age bins in the HI group compared to age matched controls.

A one sample t-test was used to compare the phoria values obtained in the HI sample with the population-based norms in the previous literature (mean phoria: −1.7 PD; range 0–3 exo) [17-21] and this was also found to be statistically significant (one-sample t-test p < 0.001).

4 Discussion

In evaluating ocular health among school children, refractive error estimation plays a major role in identifying the visual problems and their visual activities. But equal importance must be given to assessing the binocular vision anomalies which also affect their reading performance and attention span. A larger exophoria at near working distance can be a sign of convergence weakness or convergence insufficiency [11, 22]. The most common NSBVA among children were found to be CI and Accommodative Insufficiency based on recent population-based estimates in school children [8]. While most past studies in this area focused on refractive errors and ocular morbidities directly associated with deafness such as Pigmentary retinopathy in Usher's Syndrome [9, 23], this study concentrates more on the binocular visual status and co-ordination of the visual system. A review of literature shows that there is an overall lack of evidence in respect of ophthalmic problems in deaf children. Despite the prevalence of visual disorders and anomalies being as high as 40%–60%, many of these problems stay undetected for years, having a serious impact on deaf children and their communication skills [24].

Few studies conducted previously give insight on the necessity of ocular examination for deaf children. The studies conducted by Guy et al. and Nikolopoulos et al. recommend that all deaf children should have a specialist ophthalmic examination as soon as the diagnosis of deafness is confirmed, irrespective of age [9, 24].

In a study by Hollingsworth et al. (2015), the visual performance and effect of colour layers while reading were studied. The result showed that the deaf participants had greater ametropia, a more receded NPC and a reduced amplitude of accommodation compared with the hearing participants [8].

Another study showed that hearing impaired children are at greater risk of ocular morbidity. In a study of 279 children, 28% of them had some ocular morbidity and 16.5% had refractive errors. Despite having refractive errors, 78% (36 participants) did not have corrective lenses [25].

From this study sample, near phoria in deaf children was found to be −3 ± 5 Δ which is significantly higher than that of control group (−1 ± 3 Δ). Also, the prevalence of Convergence insufficiency was significantly higher in the deaf group which is similar to the results obtained by Hollingsworth et al. [8]. Prevalence of receded NPC was also higher among the HI group (10 ± 5 cm) when compared with the age matched participants (6 ± 5 cm).

The study included children in the age range of 6–15 years which is known to involve significant visual development that is known to differ between children with and without hearing impairment [26]. Further analysis between the 6–10- and 11–15-years age group did not show significant developmental trends for near point of convergence and near phoria in both the typically developing and children with hearing impairment. The differences in phoria and near point of convergence between children with and without hearing impairment continued to exist in both the age groups suggesting that developmental trends did not impact the prevalence of binocular vision dysfunctions in children with hearing impairment.

Higher prevalence of NSBVA among the deaf participants leads to more questions about the development of the visual system and the auditory feedback mechanisms. Other associations such as Usher's syndrome which drastically affect vision are known, but other features of functional vision as in visual perception and visual processing are yet to be studied. Since majority of information acquisition is via vision, and hearing with tactile and olfactory sense playing minor roles, deafness along with visual disabilities prevents the children with hearing impairment from attaining normal educational and social development. The attention span and perceptive abilities for written or typed letters is often reduced among the deaf children [27]. This is due to the fact that children with congenital sensory-neural deafness are taught with the help of both sign language and written text where auditory input is absent [28]. So they ultimately rely on visual perception to understand the signs and facial expressions of people to understand and communicate accordingly. Children with hearing impairment are known to have reduced reading vocabulary and below average mathematics performance due to difficulty in language acquisition abilities [29]. So, in general they are found to be spending lesser time engaging in activities such as reading. The implication of these visual behavior differences in light of the results obtained in the study needs further exploration.

Furthermore, need for specialized communication makes it necessary to rely only on objective responses in case of vision assessment in deaf children and a trained professional who can communicate in sign language is necessary to make sure the information regarding the tests or the condition is explained completely. What this study points out is that visual disabilities should be given a higher priority and treated before it leads to severe complications such as binocular vision dysfunctions and amblyopia.

This study does have certain limitations. Though objective parameters of vergence such as phoria and convergence status were assessed, subjective presence of symptoms could not be reliably elicited among the HI group. Also, additional accommodation parameters were not assessed, and so one cannot comment about the presence of any accommodative co-morbidities. Also, the results cannot be extrapolated to refractive groups as children who enrolled into the study were primarily emmetropes.

Children with hearing and speech impairment enrolled in the study belonged to a low-income background and were offered free education through a trust in the schools where the vision screening was offered. None of the children had additional physical disabilities or known cognitive disabilities, or intellectual disability except for the hearing and speech impairment. So no details of the level of impairment, details regarding intelligent quotient, and further medical history could be accessed.

This study has compared the phoria measures between the two study groups as assessed using modified Thorington method in the control group compared to prism cover test in children with HI. As children with HI found the modified Thorington to be more difficult and subjective responses were time consuming and unreliable, we chose the prism cover test in this group. As literatures have well established the agreement between the two methods [13, 14, 30] and the observed differences are reported to be clinically agreeable, this methodology was justifiable. Also, the receded near point of convergence in children with HI correlates with the larger exophoria ranges observed, and thus the observed differences in phoria between the two study groups can be attributed to the true difference between the groups rather than the test-driven differences.

A key aspect of binocular vision screening is to detect receded NPC and near exophoria as treatment can be offered to ease asthenopic symptoms. Treatment is cheap and effective and can aid Children's educational progression.

5 Conclusion

This study highlights the higher prevalence of receded near point of convergence and large near exophoria in children with hearing and speech impairment. Further studies to assess the perceptual abilities and visual attention of deaf children can be done to better understand the physiological effects of deafness on visual perceptual skills.

Author Contributions

Jameel Rizwana Hussaindeen: conceptualization, investigation, methodology, writing – original draft, writing – review and editing, formal analysis, supervision, resources. Mariza Mavroidis: investigation, methodology, writing – original draft, formal analysis, data curation. Badrinath P. Ashwin: writing – review and editing, formal analysis, data curation. Meenakshi S. Sruthi: investigation, project administration. Baskar Theagarayan: conceptualization, investigation, writing – original draft, methodology, writing – review and editing, formal analysis, project administration, supervision.

Ethics Statement

This study protocol was assessed and approved by the institutional ethics committee at Vision Research Foundation, Chennai, India.

Conflicts of Interest

The authors declare no conflicts of interest.

Transparency Statement

The lead author Baskar Theagarayan affirms that this manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned (and, if relevant, registered) have been explained.