|Year : 2013 | Volume
| Issue : 3 | Page : 189-201
Clinical balance tests for evaluation of balance dysfunction in children with sensorineural hearing loss
Eman A.F. Said
Audiology Unit, Department of Otolaryngology, Assiut College of Medicine, Assiut, Egypt
|Date of Submission||13-Aug-2012|
|Date of Acceptance||09-Feb-2013|
|Date of Web Publication||11-Jun-2014|
Eman A.F. Said
MD, Audiology Unit, Department of Otolaryngology, Assiut College of Medicine, 71526 Assiut
Source of Support: None, Conflict of Interest: None
Children with hearing impairment may have a potential risk for vestibular dysfunctions. They may undergo a sensory redistribution process whereby visual and somatosensory information becomes more essential for postural control. The aim of the study was to assess the balance ability in children with sensorineural hearing loss (SNHL) compared with normal-hearing controls using clinical balance subset tests. A second aim was to determine the prognostic value of some etiological, audiological, and demographic (age and sex) factors in predicting a possibility for vestibular impairment for the early identification of children with vestibular deficits.
Participants and methods
Thirty children with normal hearing (17 girls and 13 boys) and 50 children with bilateral SNHL of varying degree, aged between 5 and 15 years, were recruited from the Audiology Unit of Assiut University Hospital. All of them were subjected to the following: basic audiological evaluation (pure tone, speech audiometry), immittancemetry and auditory brainstem responses, clinical balance subset tests of the standardized Bruininks-Oseretsky Test of motor proficiency (BOT-2), modified Clinical Test of Sensory Interaction for Balance (mCTSIB), one-leg stand (OLS), and tandem stand.
Hearing-impaired (HI) children showed bilateral SNHL of varying degree, ranging from moderate to profound hearing loss (moderately–severe 32%, severe 18%, and profound 50%) and of different etiologies (heredofamilial 46%, acquired 38%, not known 16%).
Balance abilities as measured in this study were significantly poorer in HI children compared with normal-hearing children. HI children with acquired cause and profound degree of SNHL had the highest abnormal score in these clinical tests compared children with other etiologies and degrees of SNHL (although this difference did not reach statistical significance).
In most clinical balance tests that were done in this study, the youngest children in the HI group achieved scores that were almost lower than the scores obtained by the older age groups; the most significant difference was observed for tests performed with eyes closed.
Balance dysfunction occurs in a significant percentage of HI children and may have significant detrimental effects on motor development mainly in very young children. Therefore, information on the identification and treatment of these balance dysfunctions is crucial.
Keywords: balance dysfunction, prognostic factors, sensorineural hearing loss
|How to cite this article:|
Said EA. Clinical balance tests for evaluation of balance dysfunction in children with sensorineural hearing loss. Egypt J Otolaryngol 2013;29:189-201
|How to cite this URL:|
Said EA. Clinical balance tests for evaluation of balance dysfunction in children with sensorineural hearing loss. Egypt J Otolaryngol [serial online] 2013 [cited 2017 Dec 14];29:189-201. Available from: http://www.ejo.eg.net/text.asp?2013/29/3/189/134175
| Introduction|| |
Disturbances in cochlear function, which can result in sensorineural hearing loss (SNHL), could accompany vestibular impairment because the cochlea and the vestibule share the continuous membranous labyrinth of the inner ear. Therefore, injury or trauma prenatally, perinatally, or postnatally may cause damage to one or both systems 1–3. As damage to vestibular structures is known to cause balance deficit, which may interfere with normal motor development, it has been postulated as the primary cause of motor deficit 4,5. Balance control is a fundamental prerequisite for motor development in children 6.
Newborns are screened for auditory capability before discharge from the hospital. As a result, congenital and early-onset SNHL in children is usually well managed and most parents are prepared for the choices at hand for communication purposes during this most important period of development 7. Early intervention programs allow HI children approach with their normal-hearing (NH) peers with respect to speech, language skills, cognitive and social development, and academic performance. Those who are identified late often never reach the same level of skill. The critical period of postural control development is between 4 and 6 years of age; hence, intervention addressing the motor deficits in this population should be initiated before this age 8,9.
Teachers and parents of these children often report coordination difficulties, clumsiness, and balance deficits, which may hinder the child’s optimal performance 10. Moreover, many pediatric healthcare providers are often too busy or inadequately trained to conduct elaborate developmental screening tests during regular clinic visits. There are a variety of reasons why vestibular evaluation is not routinely performed in the pediatric population 11–14, with one reason being the lack of feasible and effective procedures for clinical use. Moreover, in developing countries early detection poses a significant practical challenge.
The labyrinths are known to play a role in postural responses. Therefore, it can be believed that their hypofunction would lead to delays in the acquisition of gross motor milestones. Whereas failure to acquire language skills alerts us to hearing disorders, failure to achieve motor milestones should alert us to potential vestibular dysfunction 15.
Postural or balance control is an essential prerequisite for most daily life activities in children. It is the complex ability to maintain, achieve, or restore a state of balance while a person is stationary, preparing to move, in motion, or preparing to stop moving 16–18. Afferent input from the visual, vestibular, and proprioceptive systems are integrated and evaluated by central processing systems to generate motor responses that keep the body in balance 19.
Several studies on motor skills in children with hearing impairments have shown deficits in balance, general dynamic coordination, physical fitness, and ball-catching abilities, as well as clear differences in reaction times and speed of movements 20–24. Another study reported that the onset of hearing impairment (congenital vs. delayed) has an impact on balance and manual skills and overall motor development 25. Children with hearing impairments, with a potential risk for vestibular dysfunctions, may undergo a sensory redistribution process whereby visual and somatosensory information becomes more essential for postural control, as their vestibular input may be disturbed or even absent 26–28.
In clinical practice, assessment of postural stability typically involves evaluation of functional tasks with balance constraints such as standing on one foot or walking on a balance beam. These tasks are often part of a more general motor test such as Bruininks-Oseretsky Test of motor proficiency (BOT-2) 29. The balance subset of BOT-2 [Table 1] appears to be particularly well suited to identify vestibular dysfunction in children with SNHL compared with a number of other clinical tests 30. Several studies agree that deaf individuals display inferior static and dynamic balance compared with NH individuals 31,32.
|Table 1: Balance Subtest scores of the Bruininks-Oseretsky Test of motor proficiency|
Click here to view
The balance subset of BOT-2 is a simple and cost-effective tool requiring only 10 min to administer; however, one concern is that the minimum age of administration is 4 years. Computerized dynamic posturography is certainly an alternative to BOT-2 and likely provides additional information; however, it is more costly and does not allow the assessment of very young children. BOT-2 has allowed us to accurately identify which children with SNHL suffer from concurrent abnormalities in balance 33.
The modified Clinical Test of Sensory Interaction for Balance (mCTSIB), 34,35 unilateral stance, and tandem stance on a force platform were selected to be able to evaluate sensory and motor strategies under conditions of increasing balance constraints. The duration of one-leg stand (OLS) in most motor assessment tools 29, 36, 37, is used as a static balance measure and has shown good reliability in a well-designed protocol 6,38. In a clinical setting, without the opportunity to use posturography, assessment of postural stability typically involves evaluation of functional tasks with balance constraints. The mCTSIB, unilateral stance, and tandem stance were selected to be able to evaluate sensory and motor strategies under conditions of increasing balance constraints 34,35.
The mCTSIB 33,39 allows evaluation of the influence of various sensory conditions on postural sway. By closing the eyes or by standing on a cushion, inaccurate visual and somatosensory input is provided to the central nervous system. A previous study 34 showed moderate reliability for mCTSIB, whereas another study 35 demonstrated excellent reliability for mCTSIB. These motor strategies can be evaluated not only in stance but also under more challenging conditions with a narrow base of support such as OLS or tandem stand.
These tests, one-leg stand with eyes open (OLS EO) and one-leg stand with eyes closed (OLS EC), cannot be relied upon as ideal measures of postural mechanisms. Interpretation of the results of these tests is complicated by the interplay between activity from proprioceptors, cutaneous receptors, activity from the labyrinth, and the optical righting reflex in the case of standing balance with eyes open. Less influence from nonlabyrinthine receptors occurs with standing balance with eyes closed, which eliminates the effects of visual perception. Ayres 40 found that OLS EC loaded more strongly than OLS EO on posturalocular factors 12.
As routine screening in HI children does not include assessment of balance and motor deficits, physical therapy services are not included in the education program, unless obvious neurological or orthopedic disorders are diagnosed 41.
Despite reports that, as a consequence of vestibular deficits, children have poor gaze stability that affects reading 28 and causes impairment of motor development and balance 30, 42, 43, children are typically not screened or evaluated for vestibular deficits. Consequently, vestibular dysfunction in childhood is an overlooked entity 20, and intervention to ameliorate these impairments is not provided. Hence, we aim to provide a concise description of balance and motor performance in HI children.
| Aim of this work|| |
The aim of the study was to evaluate the balance abilities of children as measured in this study using clinical tests such as the balance subset of BOT-2, mCTSIB, OLS, and tandem stand and determine the prognostic value of some etiological, audiological, and demographic(age and sex) factors associated with SNHL in predicting a possibility for balance impairment for very early identification of children with vestibular deficits, thus allowing proper counseling and recommendation for their parents.
| Participants and methods|| |
The control group comprised 30 children with NH, of whom 17 were girls and 13 were boys.
The study group comprised 53 children with a bilateral hearing loss of more than 45 dB hearing level (HL) with varying degrees and etiology of hearing impairment (hereditary, acquired, and unknown). Three of them did not complete the battery of tests and hence only 50 children (27 girls and 23 boys) were included. Forty-two children had been fitted with bilateral conventional hearing aids, five with monaural hearing aids, and three children had no hearing aids.
All children were between 5 and 15 years of age and of average intelligence (a score of 80 or higher on a standard Stanford–Binet test of intelligence). They were recruited from the Auditory Department, Assiut Medical University, with bilateral hearing impairment.
Children with neuromotor or orthopedic dysfunctions or who were taking medication affecting the central nervous system were excluded from the study. Informed consent was obtained from the parents of all participants. The study was approved by the Ethics Committee of Assiut Medical University.
Each child was submitted for:
- Each child was submitted to a careful systematic history-taking procedure with focus on vestibular and hearing complaints and physical otoneurological development.
- They also underwent a basic audiological evaluation with an audiogram made available recently for all children with hearing impairment. Behavioral (puretone) audiometry, which included air and bone conduction thresholds, speech audiometry, and tympanometry were performed to confirm normal middle ear pressure and mobility before VEMP testing. Auditory brainstem responses was also used when deemed necessary to establish or confirm hearing loss. The examination was carried out in a standard sound-proof room. SNHL was classified according to the degree of hearing loss 44. A previous study 45 had proposed an etiologic classification that clarifies the interaction between time of insult, cause, and time of expression of hearing loss 46.
Clinical evaluation of vestibular function
The ability to remove and alter sensory inputs such as vision and proprioception allows for the assessment of the relative contributions of different sensory inputs and maintenance of balance in a given patient 47. A number of clinical maneuvers exist to assess static and dynamic balance ability and sensory organization ability:
- The standardized BOT-2.
- The mCTSIB.
- The OLS test.
- The Tandem stand test.
Testing instructions were explained using total communication to ensure understanding of the activities required. Total communication consisted of sign and oral language, as well as demonstration. Instructions were repeated until the child knew what was expected of him or her, as outlined by Long 48. The investigator initially demonstrated the stance position directly in front of the child and then moved to the child’s left side. As verbal clues could not be optimally used, the investigator had to stay within the child’s visual field.
The standardized Bruininks-Oseretsky Test of motor proficiency
The balance subset of BOT-2 assesses static and dynamic balance.
A number of balance subtests of the motor proficiency test (BOT-2) 29 contain nine balance-related tasks performed either with eyes open (EO) or with eyes closed (EC) [Table 1].
The following tests comprise the group of balance subtests of BOT-2:
(1, 2) The participant stands with feet apart on a line while looking at a target on the wall and then repeats the exercise with EC. The test is stopped after 10 s.
(3) The participant walks forward on a line drawn on the floor using a normal stride and with both hands on the hips. This test is scored in a maximum of six steps. If the participant places one foot or both feet completely off the line before covering the six steps, the test is stopped and the number of successful steps is recorded (raw score).
(4, 5) The participant stands on his or her preferred foot on a line drawn on the floor while looking at a target on the wall. Both hands are on the hips, and the free (not preferred) leg is flexed at the knee; these steps are then repeated with EC. The raw score is typically the timed duration for which the child maintains the position for a maximum of 10 s.
(6) The participant walks forward on a line on the floor, heel-to-toe. Both hands are on the hips.
In tests 4–5 the trial is stopped after 10 s and the time is recorded. The trial is stopped before 10 s if the participant touches the free leg to the floor, drops the free leg below a 45° angle, hooks the free leg behind the supporting leg, or shifts the supporting foot out of place.
P is incorrect if one foot or both feet are placed completely off the line or beam, the heel of the front foot fails to touch the toe of the rear foot, or the toe of the rear foot is moved forward to touch the heel of the front foot.
The balance subtests of BOT-2 are carried out in a room free from distractions 21.
In this work, children with NH and those with SNHL were assessed only with tests 1–6. Tests 7–9 were not carried out as equipment was not available.
Raw scores were converted to point scores as described in the BOT-2 manual. Point scores are used in BOT-2 to convert raw scores (i.e. seconds vs. steps) to a common set of values. To determine the presence of a balance deficit, the mean point score of each age group was compared with the mean point score of the appropriate normative data from the BOT-2 33.
Due to lack of equipment it was marked (imp) standing for impossible 49.
The total point score and the participant’s age are used to obtain an age-matched scale score based on the scores obtained by NH children on the test (0–36 points) [Table 1]. This normal group overlapped with a previously published study 27.
The modified Clinical Test of Sensory Interaction for Balance
General instructions: the participants have to remove their shoes, stand erect without moving, and look straight ahead as long as possible or until the trial is over.
The mCTSIB is performed with the individual’s feet placed side by side with ankle bones touching, arms across his/her chest, and hands touching his/her shoulders. The mCTSIB consists of four standing positions: on a firm surface with EO, on a firm surface with EC for 30 s 49, on a foam cushion with eyes open to assess the patient’s ability to use input from the somatosensory system to maintain balance (visual aids lacking), and on a foam cushion with eyes closed to assess the patient’s ability to use input from the visual system to maintain balance (incorrect somatosensory information). The patient’s ability to use input from the vestibular system to maintain balance (other information lacking or incorrect) was also assessed. The same 45×45×18 cm, high-density, viscoelastic foam cushion was used for the last two conditions.
For the EO trials, the participants were instructed to look at a target placed at eye level in front of the platform. For the EC trials, they were asked to look at the same target before firmly closing their eyes. The safety of the children was ensured by an observer. The timing of the task was stopped when the participant’s arms moved from the original position, or when their foot moved, or when they opened their eyes during EC trial.
The OLS is a frequently used clinical assessment tool for balance to test the integrity of some postural mechanisms. In the present study a standardized protocol was used 38. The children were instructed to stand on one leg (OLS) as long as possible for a maximum of 10 s for each trial. They were barefoot, had their hands on their hips, and were made to look straight ahead. The child was then instructed to lift the right foot.
Imbalance was defined and the test was discontinued if the child placed the lifted foot on the floor, removed either hand from hips to regain balance, hopped, or moved the weight-bearing foot 50. The child was allowed one training trial before data collection. The test was then performed twice both with EO and with EC. The interval between trials for both OLS EO and OLS EC was sufficient; the child assumed a stable position with both feet on the ground and hands at his or her sides before attempting a second trial.
Two trials were performed for the left foot and the right foot both with EO (OLS EO) and with EC (OLS EC) (the scores of the two trials were added up and the average was obtained) 38.
Test manuals suggest that the outcomes of these tests (e.g. the length of time the child can SOL) provide information on the child’s general ‘balance ability’ 34, 35, 51.
The children were instructed to stand with a heel-to-toe gait and both hands on the hips. A step is incorrect if one foot or both feet are placed completely off the line, the heel of the front foot fails to touch the toe of the rear foot, or if the toe of the rear foot is moved forward to touch the heel of the front foot.
The tandem stand test was performed in two trials of 10 s each. The participants were tested barefoot or wearing soft-soled shoes and were instructed to stand as steady as possible with their arms by their sides. During each trial, the foot position remained the same because the foot position was marked.
The child’s balance ability on the mCTSIB, OLS EO, OLS EC, and tandem stand tests was determined to be normal or abnormal by comparison with standardized norms. The results of these tests were broken down according to their different cutoff limits (cutoff limit or the lowest score defined as normal=mean of the number of seconds that the normative sample was able to balance on one leg −2 SD) into children who showed scores at or above the cutoff limit and thus considered successful in these tests, and children who failed to pass the test if they scored below this cutoff limit.
All test sessions took place in the same quiet room to minimize any noise or other disturbances. At least one break was offered to the children between tests.
- Dual channel clinical audiometer (Madsen OB 922, GN Otometrics, Cobenhagen, Denmark).
- Immitancemeter (impedance audiometer AZ 26, Interacoustics AZ 26, Denmark).
- Sound-treated booth (industrial acoustic company IAC model 1602-A-t, USA).
- Nicolit Spirit equipment (USA) for electrophysiological testing (auditory brainstem responses).
- Four-channel electronystagmograph (ENG version Micromedical ENG device, version 8.1 R, USA) for the electronystagmography test.
- Navigator Pro evoked potential system manufactured by Bio-Logic (Mundelein, Illinois, USA) for the VEMP test.
Data collected were analyzed using computer program SPSS ‘version 17’ (SPSS Inc, Chicago, Illinois, USA) and expressed as mean±SD. The t-test was used to determine significance for quantitative variables and the χ 2-test to determine significance for qualitative variables. The Pearson correlation test was used for the numeric variables in the same group and the analysis of variance test for numeric values with other qualitative variables.
P values greater than 0.05 were considered nonsignificant, P values less than 0.05 were considered significant, and P values less than 0.001 were considered highly significant.
| Results|| |
Results of the basic audiological evaluation
All the children in the control group had normal developmental milestones and displayed bilateral NH. In contrast, 11 of 50 HI children had delayed milestones as their parents reported that they showed a delay in walking of more than 18 months. They showed bilateral SNHL of various degrees ranging from moderate to profound hearing loss on audiometry and with various etiologies [Table 2].
|Table 2: Demographic information of children with sensorineural hearing loss|
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Results of clinical evaluation of vestibular function
The results of the present work indicate that when children with SNHL are challenged by sufficiently difficult balance tasks that emphasize the contribution of the peripheral vestibular system, as when vision and surface inputs are eliminated and/or inaccurate, they experience difficulty in maintaining balance compared with NH children of the same age.
As noticed in [Table 3] there are statistically significant differences between NH children and HI children on using different tests for clinical evaluation of vestibular function (BOT-2, mCTSIB, OLS, and tandem stand) mainly when vision is eliminated. Meanwhile, no statistically significant differences were found in subtest 3 of BOT-2 and in the tandem stand test with EO.
|Table 3: Comparison between the mean±SD of balance subtest scores of Bruininks-Oseretsky Test of motor proficiency (point score), modified Clinical Test of Sensory Interaction for Balance, one-leg stand, and tandem stand in normal-hearing and hearing-impaired children|
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The impact of etiology of hearing level on the results of clinical tests for vestibular system assessment: Bruininks-Oseretsky Test of motor proficiency, modified Clinical Test of Sensory Interaction for Balance, stand on one leg, and tandem stand
Generally, children with hearing loss of acquired etiology displayed poorer balance performance scores compared with their counterparts with hearing loss of unknown or heredofamilial etiologies in some items of BOT-2 [Table 4], as well as in mCTSIB, OLS, and tandem stand tests, although this difference did not reach a statistically significant level between various etiologies of SNHL when compared with the results of different tests for clinical evaluation of the vestibular system.
|Table 4: Comparison between the mean±SD of balance subtest scores of Bruininks-Oseretsky Test of motor proficiency (point score) in hearing-impaired children according to various etiologies of hearing loss|
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In this study, the etiology of HL was not significantly correlated with balance as estimated by the BOT-2 score. Hence, the differences in balance abilities across various etiologies revealed that etiology may not be considered a predictor of balance abilities in HI children. It could be explained by age at onset – whether since birth or after 2 years.
Impact of the degree sensorineural hearing loss on the results of clinical tests for balance evaluation
Children with a profound degree of HL had poorer balance performance scores in the BOT-2 balance subtests compared with their counterparts with hearing loss with other degrees of SNHL [Table 5].
|Table 5: Comparison between the mean±SD of balance subtest scores of Bruininks-Oseretsky Test of motor proficiency (point score) in hearing-impaired children according to various degrees of hearing loss|
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The lowest success rates in mCTSIB, OLS, and tandem stand were achieved in HI children with a profound degree of HL compared with children with other degrees of SNHL. There were no statistically significant difference in the results of different tests for balance evaluation on the basis of degree of SNHL.
Impact of age on the results of clinical tests for balance evaluation
To study the effect of age the control group was divided according to age (5–7, 8–10, and 11–15 years) into subgroups 1, 2, and 3. The study group was also divided into three subgroups 4, 5, and 6.
HI children achieved statistically significantly poorer scores in some balance subtests of BOT-2 compared with NH children of the same age group. Meanwhile, the youngest children in both the NH and HI groups (6–7.5 years) achieved the lowest balance subtest scores and the lowest score in OLS with EO and with EC. The older age groups achieved better scores. There were statistically significant differences only in HI children with respect to the results obtained on OLS with EO (P=0.02), SOL with EC (P=0.01), and walking forward heel-to-toe on a line (P=0.01) [Table 6].
|Table 6: Comparison between the mean (SD) of balance subtest scores of Bruininks-Oseretsky Test of motor proficiency (point score) in normal-hearing and hearing-impaired children according to age|
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In mCTSIB, the youngest children in the HI group had the lowest success rate and there were statistically significant differences in HI children only with respect to the results of standing on a firm surface with EC (P=0.02) and standing on a foam cushion (P=0.009) with EC. The same result was observed for the OLS and tandem stand tests [Table 7].
|Table 7: Number and percentage of normal-hearing and hearing-impaired children who successfully passed different skill tests of modified Clinical Test of Sensory Interaction for Balance according to their age and sex|
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A HI child was considered to have successfully passed the different skill tests of mCTSIB by comparing the results with standardized norms. The cutoff limit in these tests, or the lowest value that was defined as normal, was determined as the mean number of seconds that a normal child could maintain balance −2 SD. Children were considered to have failed the test if their score was below this cutoff limit.
The impact of visual cues on performance in different clinical tests for vestibular system assessment
All HI children performed poorly in different balance skill tests and experienced greater difficulty on an identical task with their EC versus EO. The most significant effect of vision was seen in the youngest age group among both NH and HI children (groups 1 and 4) but only for tests of BOT-2 [Table 6], mCTSIB [Table 7], OLS, and tandem stand performed with EC [Table 8]. This indicates the importance of visual cues in the maintenance of balance at this young age, which seemed to apply not only for HI children but also for NH children.
|Table 8: Number and percentage of normal-hearing and hearing-impaired children who successfully passed different skill tests of one-leg stand and tandem stand tests, according to age and sex|
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Further, there were low success rates in the balance subtest that were almost lower than the success rates achieved by older HI children when compared with NH children.
The impact of sex on performance in different clinical tests for vestibular system assessment
Low success rates were achieved in both sexes of HI children when compared with NH children of the same sex with respect to different clinical tests of balance. There was no statistically significant difference between the number of poorly performing boys and poorly performing girls in both the NH and HI group with respect to the performance in different clinical tests for vestibular system assessment [Table 7] and [Table 8].
| Discussion|| |
Some studies have suggested that the clinical course of SNHL may be aggravated if the vestibular system is also involved 52,53. It may even result in delayed motor development in children 11.
This study showed that HI children performed worse in different balance skill tests (BOT-2, mCTSIB, OLS, and tandem stand) compared with NH children [Table 3]. This agrees with the study by Lindsey and O’Neal 39, who found that deaf children performed more poorly in static and dynamic balance skill tests compared with NH children.
Further, the results of other investigations 5, 6, 15, 16, 28, 39, 41, 54 have shown that children with hearing loss have a balance and/or motor deficit that may be progressive 15. As damage to the vestibular structures is known to affect motor and balance ability, many deaf children were found to have poor static balance skills in some studies 34,51.
Gheysen et al. 24 showed that NH children performed significantly better than deaf children and that hearing status had a significantly important impact mainly on the OLS test; deaf children were far less skilled than their NH peers in maintaining balance when standing on one leg. The motor skills of NH children were significantly better for all scales of the OLS. In a cross-sectional study it was found that HI children with sensory organization deficits have poor balance and motor deficiency in many areas 29.
Possible explanations for the observed motor deficits in deaf children can be enumerated 20 on the basis of four categories: (a) organic factors – associated vestibular or neurological defects; (b) sensory, auditory deprivation; (c) verbal, language deprivation – lack of verbal representations of motor skills, verbal–conceptual strategies to support execution; and (d) emotional factors – lack of self-confidence or overprotection or neglect on the part of parents, causing the deaf child to be less willing to explore the environment.
Other investigators 39, 55, 56 have reported impaired balance in deaf children because of the previously described possibility of vestibulocochlear dysfunction causing poor performance in tests on balance ability. Lack of complete comprehension of test instructions by the deaf child may be an additional cause of poor performance on the balance subtests. Hence, this study attempted to minimize the lack of comprehension using total communication and permitting one practice trial for each test.
This was not in accordance with the approach adopted in other studies 57, 58, which have emphasized that not every deaf child has a balance deficit. They reported that preimplant motor scores of prelingually deaf infants and children fell within the typical range of variation found in NH children. Rapin 59 also described a delay in motor development in some, but not all, children with limited vestibular function included in her study.
Horak et al. 42 found that they could not differentiate the control group from the HI group despite the presence of reduced peripheral vestibular function in HI patients (one-foot stand, both with EO and with EC) 54–56. A lack of universal findings on balance deficits and deafness suggests that some deaf children simply do not have a deficit, whereas others may have a deficit but use other sensory systems to compensate 60.
Impact of etiology of sensorineural hearing loss on the results of clinical tests for vestibular system assessment
In this study, it was noticed that HI children with acquired etiology of deafness performed poorly in different balance skill tests of BOT-2 [Table 4], mCTSIB, OLS, and tandem stand tests, compared with children with other etiologies.
This result agrees with that of Potter and Silverman 60, who suggested that children born deaf are less likely to have a balance dysfunction compared with those who acquire deafness, usually secondary to meningitis, in infancy or during early childhood. Also, other studies reported that the lower level of balance in deaf children can be attributed to vestibular defects, most often related to cerebral meningitis 50, 61, 62.
This also agrees with the results of a previous study, which reported that those whose cause of deafness was meningitis suffer from the most serious balance deficits 54.
Cushing et al. 33 also found that children with deafness caused by meningitis or cochleovestibular anomalies display poorer balance than those with mutations in the GJB2 encoding connexin 26 gene or with SNHL of unknown etiology, although the latter two groups also contained a number of poor performers. However, this was not in agreement with the results of another study 63 that suggested that the cause of deafness appears to have only a negligible influence on postural stability.
In this study, there was no statistically significant difference in the results of different tests for clinical assessment of the vestibular system on the basis of differences in etiology of SNHL. This agrees with the results of Boyd 63 who also reported no significant differences in static equilibrium ability on the basis of the etiology of deafness. However, this did not agree with the results of other investigators 64 who found that balance ability was significantly correlated with etiology.
Impact of the degree of sensorineural hearing loss on the results of clinical tests for vestibular system assessment
In this study HI children with profound SNHL tended to perform more poorly, as reflected by their low scores in all subtests of BOT-2 [Table 7], compared with children with other degrees of SNHL, although there was no statistically significant difference in the results of different tests for clinical evaluation of the vestibular system assessment on the basis of differences in the degree of SNHL. Also, the lowest success rate was achieved in HI children with profound SNHL in all subtests of mCTSIB, SOLS, and tandem stand tests [Table 5].
This agreed with the results of other studies, which reported a high prevalence of poor performance on tasks of standing balance in a profoundly deafened cohort 59, 60, 65. Schwab and Kontorinis 64 concluded that the extent of hearing loss alone does not enable conclusions to be drawn about either vestibular function or dynamic balance performance.
Impact of vision on the results of clinical tests for vestibular system assessment
This study demonstrated the impaired balance in HI children as reflected by their lower scores in all subtests of BOT-2 [Table 4] and lower success rate in the mCTSIB, OLS, and tandem stand tests with the elimination of visual input [Table 5] and [Table 6].
This was consistent with the results of another study 66 that reported that deaf children with vestibular loss could not maintain balance in the standing position when the visual input was removed and the somatosensory input was modified. Yet, when visual and somatosensory input was enabled, these children showed postural control similar to that of deaf children with normal vestibular function and that of hearing children. This suggests a compensation process whereby input from proprioceptive, visual, and other sensory systems substitute for the absent peripheral vestibular input.
This finding also agreed with the findings of researchers 24 who suggested that hearing status had a significantly important impact mainly on the OLS test and that deaf children were far less skilled than their NH peers in maintaining balance when standing on one leg especially with EC. Potter and Silverman 60 showed that many deaf children seemed to compensate for vestibular deficits through nonlabyrinthine systems, such as visual and kinesthetic, to maintain static balance with EO or closed.
Lindsey and O’Neal 39 also agreed that balance ability decreases in the dark and when eyes are closed. Another study 65 indicated that in situations in which vision controls movement deaf children are seen to perform better than healthy children. This is attributed to the better eye–hand coordination of deaf children, which is an outcome of the training they undergo with emphasis on visual stimuli. This disagrees with the findings of Cushing et al. 33, who demonstrated that the relative importance of vision on the maintenance of balance is unchanged in the presence of bilateral vestibular loss. This was reflected in the observation that all children, whether NH or deaf, and with or without concurrent vestibular dysfunction, suffered a proportionally identical decrement in performance on certain subtests of the BOT-2 when their eyes were closed.
Impact of age of hearing-impaired children on the results of clinical tests for vestibular system assessment
This study showed that HI children achieved lower scores when compared with NH children in different clinical balance skill tests (BOT-2, mCTSIB, SOL, and tandem stand tests) at all age groups. This agrees with the results of Myklebust 54 and was also consistent with the findings of Boyd 63, who reported that there were differences in static balance between deaf and NH boys at all ages and significant differences in dynamic balance between deaf and NH boys of 9 and 10 years of age.
In this study the success rates for HI children in the different balance subtests of BOT-2, mCTSIB, OLS, and tandem stand tests increased with age [Table 6], [Table 7] and [Table 8]. This was reflected in the lower scores in young HI children (5–7 years) when compared with the other age groups (8–10 and 11–15 years). This agreed with the results of Siegel et al. 21, who found significantly higher scores in the balance tests with increasing age, as seen when the scores of group 1 (40.5–60.5 years.) were compared with those of group 2 (8–10 years) and when balance scores of group 1 were compared with those of group 3 (12.5–14 5 years). No significant difference was found between the scores of groups 2 and 3. They noted that the youngest children achieved balance subtest scores that were almost 50% lower than the mean score of the NH population of the same age in the standardization trials. Groups 2 and 3 each had scores that were ∼20% lower than the mean score of the standardized population of the appropriate age.
This study showed that children with NH and normal vestibular function between the ages of 5–7 years typically display reduced balance ability when vision and surface inputs are eliminated and/or are inaccurate. This is consistent with the results of Shumway-Cook and Woollacott 47 and reflects the defect in the sensory organization system in young children. This was consistent the results of Butterfield 10 and Siegel et al. 21, who reported that HI children (hearing loss>60 dB) aged between 3 and 14 years tested using a version of the BOT-2 that was restricted to balance exercises showed improved postural stability consistently with increase in age.
Rajendran and Roy 67 reported that it is normal for individuals belonging to both sexes in various age groups to have a certain amount of postural sway. However, the child imitates the adult pattern of postural control by the age of 7–10 years. According to the sensory systems, young children depend on the visual system to maintain balance. As they grow older, there is progressive domination of the somatosensory and vestibular systems.
In the study by Morsh 68 an improvement was seen in the balance ability of deaf individuals only until the age of 9 years, after which no clear improvement was seen. The period between the ages of 4 and 6 is a transitional phase before the ability to resolve multimodal sensory conflicts is fully in place. Not until the age of 7 years did the child exhibit adult-like behavior in terms of postural control 48.
Schwab and Kontorinis 64 confirmed the hypothesis that attainment of balance is subject to an age-dependent maturation process. The development of balance requires that all components continually develop and adjust and, above all, that these different sensory impressions are integrated within the central nervous system, although the vestibular organ is already structurally and functionally developed by the time of birth.
Results of previous studies 1, 54, 60, 63, 69–72 indicate that, in order to compensate for balance deficits, deaf children use other sensory systems, such as proprioception, kinesthesia, and vision. This disagrees with the findings of Siegel et al. 21, who reported that the balance scores of deaf children were equidistant from the scores of NH children across age groups, which strongly suggests that the degree of compensation, when it occurs, is insufficient to diminish the balance deficit in the three age groups we examined.
The significant influence of age appears not only in studies on motor performance of deaf pupils but also of all student populations. Many researchers attributed this improvement to the increasing maturity of the central nervous system and myoskeletal development with age 64,72.
Impact of sex of hearing-impaired children on the results of clinical tests for vestibular system assessment
In this study girls and boys with HI had lower success rates compared with girls and boys with NH in the performance of different balance skill tests. This was in agreement with the results of Boyd 63, who found that deaf boys have less skill than NH boys in maintaining dynamic balance. This was an effect of SNHL and not of sex.
This study demonstrated no difference in balance skills on the basis of sex in the BOT-2, mCTSIB, SOL, and tandem stand tests. This agrees with the results obtained in previous studies 62,73 in which tests of standing balance with eyes open and closed demonstrated no difference in balance skills on the basis of sex. They noted societal trends in which girls were more likely than boys to be physically active when compared with the level of activity in 1927.
A recent study 65 found no difference in performance in terms of static or dynamic balance between deaf girls and deaf boys. This also agrees with the results of some researchers 73,74 who found no difference in the balance abilities of deaf boys and girls. No significant difference was found in standing balance skills with eyes either open or closed between girls and boys 60,68.
This disagrees with the results of several investigators who concluded that the balance ability of deaf boys was superior to the balance ability of deaf girls and they found that deaf girls swayed more than deaf boys. They used either standing balance or beam walking as tests in their studies 48,54. Some investigators have found deaf girls to sway more than deaf boys 52,74.
Some investigators believed that sex is another factor that affects balance. Deaf boys were thought to have superior balance ability compared with deaf girls, according to studies conducted in the 1930s 53.
Also, Riach and Hayes 75, who studied the maturation of postural stability in children aged between 2 and 14 years, reported that, although boys initially show greater instability than girls, they stabilize better and faster with age. One conceivable cause might be the different patterns of play between girls and boys, with boys’ play more dominated by physical activity, which aids in increasing a sense of balance.
Although several investigators 50, 56, 64 have reported impaired balance in deaf children, others have emphasized that not every deaf child has a balance deficit. Potter and Silverman 60 suggest that children who are born deaf are less likely to have balance dysfunction compared with those who acquire deafness, usually secondary to meningitis, in infancy or during early childhood. A lack of universal findings on balance deficits and deafness suggests that some deaf children simply do not have a deficit, whereas others may have the deficit but use other sensory systems to compensate. A previous study 30 used a very sophisticated system for testing vestibular function in a group of HI children before testing their motor proficiency. They found a group of HI children with normal vestibular function who performed a series of motor tasks as well as, or better than, control groups. The HI children with reduced vestibular function showed poor results on the balance subtest of the BOT-2 30.
The discrepancy could be explained by the observation that the studies by Myklebust 54, Morsh 68, and Long 48 were conducted in the 1930s, when girls typically led more protected lives and were less physically active than boys. Consequently, deaf girls may not have had the same opportunities to develop balance ability as did their male counterparts. Our findings support those of the more recent studies. We found no significant difference between male and female subjects. They believed that age-appropriate activities or exercise used to improve balance ability in deaf children did not have to be different between male and female subjects because neither sex is superior.
Butterfield and Loovis 76 found out statistically significant differences between the two sexes. In their effort to justify this difference, they accepted the theory of Greendorfer and Lewko 77 related to the acquisition of increased motion experience by boys as compared with girls, which stipulates that fathers encourage boys more to participate in sports. Anthrop and Allison 78 called this phenomenon the ‘Victorian influence’ and explained girls’ lack of participation in sports as being due to sports being considered a dangerous activity.
| Conclusion|| |
Balance abilities as measured in this study with the balance subset of BOT-2, mCTSIB, OLS, and tandem stand were significantly poorer in HI children when compared with NH children.
HI children with acquired cause of hearing loss had observable lowest scores in these clinical tests compared with children with other etiologies. In contrast, those with a profound degree of hearing loss achieved observable poorest scores, although the scores were not statistically significant from those of children with other etiologies and degrees of SNHL. The youngest HI children had the lowest balance scores, and the clearest effect was observed for tests performed with eyes closed. The sex of the participant seems to have a negligible influence on the performance of different clinical tests of vestibular system assessment in HI children.
The high incidence of vestibular dysfunction and problems with balance in HI children without other handicaps is of vital information for therapists concerned with evaluating and treating HI children. Therefore, in order to minimize the adverse effects on normal development, it is crucial to carry out vestibular screening examinations and vestibular testing in all children with SNHL.
Further, once vestibular symptoms or deficits are identified, the children should be referred for testing of balance, motor development, and gaze stability. Appropriate interventions against balance and motor deficits are warranted so that functional improvement can be achieved by participation in vestibular rehabilitation programs focused on substitution and adaptation exercises. However, additional work is needed to examine the long-term effects of intervention.
| References|| |
|1.||Pajor A, Jozefowicz-korczynsks M.Prognostic factors for vestibular impairment in sensorineural hearing loss.Ear Arch Otorhinolaryngol. 2008;265:403–407. |
|2.|| Wilson VJ, Peterson BW Mountcastle VB.The role of the vestibular system in posture and movement.Medical physiology. 1980;Vol. 1. 14th ed..St Louis, MO:CV Mosby Co.;813–836. |
|3.|| kaga K.Vestibular compensation in infants and children with congenital and acquired vestibular loss in both ears.Int J Pediatr Otorhinolaryngol. 1999;49:215–224. |
|4.|| Jongkees LB, Maas JP, Philipszoon AJ.Clinical nystagmography: a detailed study of electro-nystagmography in 341 patients with vertigo.Pract Otorhinolaryngol. 1962;24:65–93. |
|5.|| Jongkees LB.Vestibular tests for the clinician.Arch Otolaryngol. 1973;97:77–80 1973. |
|6.|| De Kegel A, Dhooge I, Cambier D, Baetens T, Palmans T, Van Waelvelde H.Test–retest reliability of the assessment of postural stability in typically developing children and in hearing impaired children gait & posture.J Gait Posture. 2011;33:679–685. |
|7.|| Windmill IM.Universal screening of infants for hearing loss: further justification.J Pediatr. 1998;133:318–319. |
|8.|| Woollacott MH, Debu B, Mowatt M.Neuromuscular control of posture in the infant and child: is vision dominant?J Mot Behav. 1987;19:167–168. |
|9.|| Woollacott MH, Shumway-Cook A.Changes in postural control across the life span – a systems approach.Phys Ther. 1990;70:799–807. |
|10.|| Butterfield SA.Gross motor profiles of deaf children.Percept Mot Skills. 1986;62:68–70. |
|11.|| Angeli S.Value of vestibular testing in young children with sensorineural hearing loss.Arch Otolaryngol Head Neck Surg. 2003;129:479–482. |
|12.|| Goebel JA.Should we screen hearing-impaired children for vestibular dysfunction?Arch Otolaryngol Head Neck Surg. 2003;129:482–483. |
|13.|| Snashall SE.Vestibular function tests in children.J R Soc Med. 1983;76:555–559. |
|14.|| Valente LM.Adaptation of adult techniques for evaluating vestibular function in children.Hear J. 2007;60:34–44. |
|15.|| Mergner T, Rosemeier T.Interaction of vestibular, somatosensory and visual signals for postural control and motion perception under terrestrial and microgravity conditions – a conceptual model.Brain Res Brain Res Rev. 1998;28:118–135. |
|16.|| Arnvig J.Vestibular function in deafness and severe hardness of hearing.Acta Otolaryngol. 1955;45:283–288. |
|17.|| Goldstein R, Landau E, Kleffner F.Neurological assessment of some deaf and aphasic children.Ann Otol Rhinol Laryngol. 1958;67:468–479. |
|18.|| Sandberg L, Terkildsen K.Caloric tests in deaf children.Arch Otolaryngol. 1965;81:350–354. |
|19.|| Buchman CA, Joy J, Hodges A, Telischi FF, Balkany TJ.Vestibular effects of cochlear implantation.Laryngoscope. 2004;114 Suppl 103 1–22. |
|20.|| Wiegersma PH, Van der Velde A.Motor development of deaf children.J Child Psychol Psychiatry. 1983;24:103–111. |
|21.|| Siegel JC, Marchetti M, Tecklin JS.Age-related balance changes in hearing-impaired children.Phys Ther. 1991;71:183–189. |
|22.|| Lieberman LJ, Volding L, Winnick JP.Comparing motor development of deaf children of deaf parents and deaf children of hearing parents.Am Ann Deaf. 2004;149:281–289. |
|23.|| Goodman J, Hopper C.Hearing impaired children and youth: a review of psychomotor behavior.Adapt Phys Activ Q. 1992;9:214–236. |
|24.|| Gheysen F, Loots G, Van Waelvelde H.Motor development of deaf children with and without cochlear implants.J Deaf Stud Deaf Educ. 2008;13:215–224. |
|25.|| Shall MS.The importance of saccular function to motor development in children with hearing impairments.Int J Otolaryngol. 2009;2009:972565. |
|26.|| Sechzer JA, Folstein SE, Geiger EH, Mervis RF, Meehan SM.Development and maturation of postural reflexes in normal kittens.Exp Neurol. 1984;86 no. 3 493–505. |
|27.|| Rine RM, Cornwall G, Gan K, LoCascio C, O’Hare T, Robinson E, Rice M.Evidence of progressive delay of motor development in children with sensorineural hearing loss and concurrent vestibular dysfunction.Percept Mot Skills. 2000;90:1101–1112. |
|28.|| Rine RM, Lindblad S, Donovan P, Vergara K, Gostin J, Mattson K.Balance and motor skills in young children with sensorineural hearing impairment: a preliminary study.Pediatr Phys Ther. 1996;8:55–61. |
|29.|| Bruininks RH, Broininks BD.Bruininks-Oseretsky Test of motor proficiency manual. 2005:2nd ed..Minneapolis, MN:NCS Pearson Inc. |
|30.|| Crowe TK, Horak FB.Motor proficiency associated with vestibular deficits in children with hearing impairments.Phys Ther. 1988;68:1493–1499. |
|31.|| Selz PA, Girardi M, Konrad HR, Huges LF.Vestibular deficits in deaf children.Otolaryngol Head Neck Surg. 1996;115:70–77. |
|32.|| Lelard T, Jamon M, Gasc J, Vidal P.Postural development in rats.Exp Neurol. 2006;202:112–124. |
|33.|| Cushing SL, Papsin BC, Rutka JA, James AL, Gordon KA.Evidence of vestibular and balance dysfunction in children with profound sensorineural hearing loss using cochlear implants.Laryngoscope. 2008;118:1814–1823. |
|34.|| Geldhof E, Cardon G, De Bourdeaudhuij I, Danneels L, Coorevits P, Vanderstraeten G, et al..Static and dynamic standing balance: test–retest reliability and reference values in 9- to 10-year-old children.Eur J Pediatr. 2006;165:779–786. |
|35.|| Gabriel LS, Mu K.Computerized platform posturography for children: test–retest reliability of the sensory test of the VSR system.Phys Occup Ther Pediatr. 2002;22:101–117. |
|36.|| Folio MR, Fewell RR.Peabody Developmental Motor Scales-2. 2000.Austin, TX:PROED. |
|37.|| Henderson SE, Sugden DA, Barnett AL.Movement assessment battery for children-2: examiner’s manual.2007.London, UK:Pearson Assessment Inc. |
|38.|| Atwater SW, Crowe TK, Deitz JC, Richardson PK.Interrater and test–retest reliability of two pediatric balance tests.Phys Ther. 1990;70:79–87. |
|39.|| Lindsey D, O’Neal J.Static and dynamic balance skills of eight-year-old deaf and hearing children.Am Ann Deaf. 1976;121:49–55. |
|40.|| Bilir S, Guvin N, Bal S, Metin N, Artan I.A comparison study of gross motor developmental skill normal, hearing-impaired and Down syndrome children. Paper presented at the International Congress on education of the deaf Tel Aviv, Israel; 1995. pp. 16–20. |
|41.|| Omondi D, Ogol C, Otieno S, Isaac macharia.Parental awareness of hearing impairment in their school-going children and health care seeking behaviour in Kisumu district, Kenya.Int J Pediatr Otorhinolaryngol. 2007;71:415–423. |
|42.|| Horak FB, Shumway-Cook A, Crowe TK, Black FO.Vestibular function and motor proficiency of children with impaired hearing or with learning disability and motor impairments.Dev Med Child Neurol. 1988;30:64–79. |
|43.|| Krebs DE, Gill-Body KM, Riley PO, Parker SW.Double-blind, placebo–controlled trial of rehabilitation for bilateral vestibular hypofunction: preliminary report.Otolaryngol Head Neck Surg. 1993;109:735–741. |
|44.|| .Degree of hearing loss. Avaliable at: http://www.asha.org/public/hearing/Degree-of-Hearing-Loss/ . |
|45.|| Davidson J, Hyde ML, Alberti PW.Epidemiology of hearing impairment in childhood.Scand Audiol Suppl. 1988;30:13–20. |
|46.|| Espeso A, Owens D, Williams G.The diagnosis of hearing loss in children: common presentations and investigations.Curr Pediatr. 2006;16:484–488. |
|47.|| Shumway-Cook A, Woollacott MH.The growth of stability: postural control from a development perspective.J Mot Behav. 1985;17:131–147. |
|48.|| Long J.Motor abilities of deaf children. Contribution to Education, no. 514.1932.New York, NY:Columbia University Teachers’ College. |
|49.|| Shumway-Cook A, Horak FB.Assessing the influence of sensory interaction on balance: suggestion from the field.Phys Ther. 1986;66:1548–1550. |
|50.|| Ayres AJ.Southern California Postrotary Nystagmus. Test Manual. 1975.Western Psychological Services: Los Angeles |
|51.|| Latash M, Hadders-Algra M Hadders-Algra M, Carlberg EB.What is posture and how it is controlled?Postural control: a key issue in developmental disorders. 2008.London, UK:Mac Keith Press;3–21. |
|52.|| Effgen SK.Effect of an exercise program on the static balance of deaf children.Phys Ther. 1981;61:873–877. |
|53.|| Doershuk CF, Mathews LW, Tucker AS, Spector S.Evaluation of a prophylactic and therapeutic program for patients with cystic fibrosis.Pediatrics. 1965;36:675–688. |
|54.|| Myklebust HR.The psychology of deafness. 1964:2nd ed.New York, NY:Grune & Stratton Inc.;180–201. |
|55.|| Scanlon SL, Goetzinger CP.The health rails and Fukuda vestibular tests with deaf and hearing subjects.Eye Ear Nose Throat Mon. 1969;48:8–15. |
|56.|| McCarron L, Ludlow G.Sensorineural deafness and neuromuscular dysfunctions: considerations for vocational evaluation and job placement.J Rehabil. 1981;47:59–79. |
|57.|| Horn DL, Pisoni DB, Miyamoto RT.Divergence of fine and gross motor skills in prelingually deaf children: implications for cochlear implantation.Laryngoscope. 2006;116:1500–1506. |
|58.|| Kutz W, Wright C, Krull KR, Manolidis S.Neuropsychological testing in the screening for cochlear implant candidacy.Laryngoscope. 2003;113:763–767. |
|59.|| Rapin I.Hypoactive labyrinths and motor development.Clin Pediatr. 1974;13:922–937. |
|60.|| Potter CN, Silverman LN.Characteristics of vestibular function and static balance skills in deaf children.Phys Ther. 1984;64:1071–1075. |
|61.|| Shephard Roy J.Fitness in special populations. 1990.Champaign, Illinois 350. |
|62.|| Brunt D, Broadhead GD.Motor proficiency traits of deaf children.Res Q Exerc Sport. 1982;53:236–238. |
|63.|| Boyd J.Comparison of motor behavior in deaf and hearing boys.Am Ann Deaf. 1967;112:598–605. |
|64.|| Schwab B, Kontorinis G.Influencing factors on the vestibular function of deaf children and adolescents – evaluation by means of dynamic posturography.Open Otorhinolaryngol J. 2011;5:1–9. |
|65.|| Cushing SL, James AL, Papsin BC, Gordon KA.The vestibular olympics: a test of dynamic balance function in children with cochlear implants.Arch Otorhinolaryngol. 2007;134:34–38. |
|66.|| Suarez H, Angeli S.Balance sensory organization in children with profound hearing loss and cochlear implants.Int J Pediatr Otorhinolaryngol. 2007;71:629–637. |
|67.|| Rajendran V, Roy FG.An overview of motor skill performance and balance in hearing impaired children.Rajendran and Roy Italian Journal of Pediatrics. 2011;37:33. |
|68.|| Morsh JE.Motor performance of the deaf.Comp Psychol Monogr. 1936;13:1–51. |
|69.|| Gallahue D.Understanding motor behavior in children. 1982.New York, NY:John Wiley Sons Inc. |
|70.|| Kandel ER, Schwanz JH.Principles of neural science. 1985:2nd ed..New York, NY:Elsevier Science Publishing Co. Inc.;584–595. |
|71.|| Padden DA.Ability of deaf swimmers.Res Q. 1959;30:214–225. |
|72.|| Kaga K, Suzuki J, Morsh RR.Influence of labyrinthine hypoactivity on gross motor developmentof infants.Ann NY Acad Sci. 1981;374:412–420. |
|73.|| Carlson RB.Assessment of motor ability of selected deaf children in Kansas.Percept Mot Skills. 1972;34:303–305. |
|74.|| Gayle GW, Pohlman RL.Comparative study of the dynamic, static, and rotary balance of deaf and hearing children.Percept Mot Skills. 1990;70:883–888. |
|75.|| Riach CL, Hayes KC.Maturation of postural sway in young children.Dev Med Child Neurol. 1987;29:650–658. |
|76.|| Butterfield SA, Loovis ME.Influence of age, sex, balance, and sport participation on development of throwing by children in grades K-8.Percept Mot Skills. 1993;76:459–464. |
|77.|| Greendorfer SI, Lewko JH.Role of the family members in sport socialization of children.Res Q. 1978;49:30–48. |
|78.|| Anthrop J, Allison MT.Roll conflict and the high school female athlete.Res Q Exerc Sport. 1983;24:104–111. |
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]