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Motor proficiency and dynamic visual acuity in children with bilateral sensorineural hearing loss
International Journal of Pediatric Otorhinolaryngology 76 (2012) 1520–1525
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Motor proficiency and dynamic visual acuity in children with bilateral sensorineural hearing loss Willemien Martin a, Jennifer Jelsma b,*, Christine Rogers b a b
University of Cape Town, South Africa Department of Rehabilitation Sciences, University of Cape Town, South Africa
A R T I C L E I N F O
A B S T R A C T
Article history: Received 27 March 2012 Received in revised form 2 July 2012 Accepted 4 July 2012 Available online 22 July 2012
Aims and objectives: Due to the close relationship between the cochlea and the peripheral vestibular system, the function of the vestibular system may be impaired in children with sensorineural hearing loss. The aims of this study were to determine the prevalence of impairments of motor performance and dynamic visual acuity, and the nature and extent of interaction between these in children with sensorineural hearing loss between the ages of 4 and 14 years. Methods: This research utilized a correlational, cross-sectional, descriptive design. Thirty-two children with sensorineural hearing loss were matched according to age and gender with children with no hearing impairment. Motor performance was evaluated by means of the Movement Assessment Battery for Children-2 and dynamic visual acuity was evaluated with the dynamic visual acuity test. The performances of the two groups on the different tests were then compared. Data analysis: The one-sided chi-square test or Fisher’s exact test was used to determine whether there was any association between sensorineural hearing loss, impaired motor performance and poor dynamic visual acuity. The Mann–Whitney U-test was used to determine the difference between children with sensorineural hearing loss and those with normal hearing on the Movement Assessment Battery for Children-2. Forward stepwise regression was used to establish the predictors of the Movement Assessment Battery for Children-2 total standard score. The Kruskal–Wallis test was used to compare scores of children with normal hearing and those with a mild to moderate sensorineural hearing loss on the Movement Assessment Battery for Children-2. Results: Reduced dynamic visual acuity is associated with sensorineural hearing loss (p = 0.026). Motor performance is dependent on dynamic visual acuity and severity of sensorineural hearing loss (r2 = 0.41, p = 0.001). Conclusions: The results of this study indicate that in children with sensorineural hearing loss, the prevalence of reduced dynamic visual acuity is 15.6% and of motor impairment is 65.6%. Both abnormal dynamic visual acuity and motor impairment are associated with sensorineural hearing loss. It is important to evaluate children with sensorineural hearing loss for the presence of abnormal dynamic visual acuity as well as motor impairment, because it can have serious implications for the safety, education and general well being of these children. ß 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Children Dynamic visual acuity Motor performance Sensorineural hearing loss Vestibular hypofunction
1. Introduction Due to the close relationship between the cochlea and the peripheral vestibular system with respect to embryology, physiology and anatomy, the function of the vestibular system may be impaired in children with sensorineural hearing loss (SNHL) [1,2]. Several authors have shown that children with SNHL are more
* Corresponding author at: Faculty of Health Sciences, Anzio Road Observatory, 7925 Cape Town, South Africa. Tel.: +27 214066401. E-mail addresses: fi[email protected] (W. Martin), [email protected] (J. Jelsma), [email protected] (C. Rogers). 0165-5876/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2012.07.007
likely to have vestibular impairment than normal-hearing children [3–9]. Despite reports of vestibular disorders in children with SNHL, the functional integrity of the vestibular system is not often tested, and any impairment may therefore go undetected and untreated [10]. One reason might be that vestibular disorders are typically perceived as problems affecting mainly adults [10]. Another reason might be the difficulty describing the sensations of a vestibular disorder. It may be impossible for children, particularly young children, to describe what they experience. This can be due to a lack of basic communication skills, especially in children with hearing loss [10]. A third reason might be that compensation can take place during childhood by using visual and somatosensory systems [2,11]. In cases where impaired vestibular
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function was compensated for by other systems, vestibular hypofunction may be misdiagnosed or not identified because children demonstrate no outward abnormalities of gait and motor coordination [12]. The function of the mature vestibular system is to stabilize the position of the eyes, head and body in space, and to assist in maintaining an upright position [1,11]. The peripheral vestibular system consists of two parts with different functions. Firstly, the vestibular-ocular system is responsible for gaze stabilization and clear vision by means of the vestibular-ocular reflex (VOR). Secondly, the vestibular-spinal system as a result of the function of the vestibular-spinal reflex (VSR), contributes to muscle tone, aids in the acquisition of motor developmental milestones and it also helps with postural control [1]. Children with congenital vestibular abnormalities often display delayed gross motor development as well as problems with static and dynamic balance [1,13]. Late acquisition of developmental milestones in children with congenital vestibular dysfunction is thought to be the result of insufficient vestibular input [2]. However, age-expected motor proficiency is often achieved by adolescence as a result of compensation, especially when the visual and somato-sensory systems are intact [1–3]. Visual tasks, such as learning to read, may be problematic for children with congenital vestibular abnormalities due to impairment of the gaze stabilizing function of the vestibular system [14]. This may impact on scholastic performance, which in turn can lead to a reduced quality of life and sub-optimal levels of education [10]. Although there are indications that motor development and bilateral vestibular hypofunction (BVH) may be related, little research has been done on the relationship between BVH and dynamic visual acuity in children with congenital or early acquired SNHL [14]. BVH is defined as the loss of tonic and dynamic input from both labyrinths or from both vestibular nerves [2]. Dynamic visual acuity refers to the ability to see clearly while the head is moving [10]. In children with hearing loss, investigation of the impact of BVH on dynamic visual acuity and reading is important, because of the increased incidence of visual and reading problems in the hearing-impaired group [14]. It has been demonstrated that children with vestibular hypofunction (VH), particularly those with BVH, have poorer reading acuity scores than peers without VH regardless of hearing status [14]. Furthermore, reading acuity scores correlated with dynamic and not static visual acuity scores. This might be due to difficulties with visual stabilization [14]. The effect of BVH on dynamic visual acuity in children with congenital or early acquired SNHL has not been established conclusively. While there is some research on the reading acuity of children with vestibular hypofunction [14], there still remain some areas that could do with better delineation, such as the effect of poor dynamic visual acuity on motor performance of children. By comparing motor performance and dynamic visual acuity of hearing-impaired children with normal-hearing peers, it may be possible to determine whether impairment of these functions is associated with SNHL. Research in this field is important to determine the prevalence of impaired motor performance and reduced dynamic visual acuity in children with SNHL in order to provide healthcare professionals with the necessary information to address these possible impairments; for example, by highlighting the need for vestibular rehabilitation therapy, which is known to target gaze stabilization effectively in adults [15]. The aims of the study were therefore, in children with congenital and early acquired SNHL, to establish the prevalence of impairments of motor performance and dynamic visual acuity. A second aim was to determine the nature and extent of interaction between these parameters.
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1.1. Research setting The study took place at a school (the School) which offers education to typically developing children and children with SNHL. This mainstream school is regard to be unique in the world because of its specific curriculum as well as the inclusion of a few children with hearing loss and with no other disabilities into regular classes where they can learn alongside their peers with normal hearing. 2. Methodology The study utilized a correlational, cross-sectional, descriptive design. 2.1. Sample A sample of convenience was utilized as the cases included only those children attending the School with SNHL and as such was not representative of the population of children with SNHL. Parental reports of their child’s neurological problems, cochlear implants in the preceding 12 months, conductive hearing loss, poor visual acuity that was not correctable, taking medication with ocular, neuro-otological or vestibular side-effects and learning disabilities resulted in the child not being invited to participate in the study. As the study was school based, the researcher did not have access to the medical records of the children and had to rely on parental report of the medical history. The sample size was based on the need to ensure that the sample was large enough to perform multiple regression analysis. Using a statistical package [16] and data from a previous study, it was calculate that a total of 52 participants needed to enroll. A total of 64 participants took part in the current study which included all eligible children with SNHL from the School. The sample of children with SNHL comprised 32 participants of which 15 were female. The mean age of the children was 9.4 years (SD 2.4, range 4.5–13.2). There were 32 normalhearing children of which 17 were males. The mean age of the participants was 9.4 years (SD 2.5, range 4.6–13.3). An audiologist of the School who was familiar with the medical history of the children and who had access to their records, selected the children with SNHL and matched them with 32 normal-hearing children according to age and gender. 2.2. Instrumentation The classification system for hearing loss in children provided by Northern and Downs [17] was used to categorize the degree of hearing loss. A pediatric scale was developed due to the vastly different effect of hearing loss in children when compared to adults [17]. Movement ability was tested using the Movement Assessment Battery for Children-2 (MABC-2), which has been reported to be a reliable and valid test of motor performance in children [18–20]. The intra-class correlations (ICC) for inter-rater reliability for the M-ABC-2 exceeded 0.95 and ranged between 0.92 and 0.98 for the test–retest reliability [21]. It includes three different components: manual dexterity, ball skills and balance. Scores are calculated using each of these components and a standard score is derived. The total test score ranges between a minimum of one and a maximum of 19; with a score of eight or more indicating that no movement difficulty is present [22]. A standard score of six or seven suggests that the child is at risk of a movement difficulty and a standard score of five or less indicates a significant movement difficulty [23]. The dynamic visual acuity (DVA) test that was adapted by Rine and Braswell [23] for use with young children was utilized in the current study. The Lea vision chart which has symbols instead of
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letters was used. Rine and Braswell [23] found that the test–retest reliability for SVA and horizontal DVA was excellent with ICC = 0.94 and 0.84 respectively as well as the inter-rater reliability with ICC for SVA = 0.93 and for horizontal DVA = 0.88. Sensitivity, specificity as well as positive and negative predictive values for BVH were 100%, regardless of age (ANOVA p = 0.007) [23]. The participant began to identify symbols on the middle line (20/200). This was continued for successive lines until the participant missed three of the five optotypes on a line. The log MAR values of this line and those of the lowest line for which all the optotypes were correct were recorded [23]. This was done under two conditions: (1) head stationary, and (2) head tilted forward with the neck in 308 of flexion and manually rotated 308 by the researcher (sinusoidally, 158 from centre to the left and to the right), to the beat of a metronome at 2 Hz (hDVA). A dynamic visual acuity score was calculated as the difference between static visual acuity (SVA) and dynamic visual acuity (hDVA) in lines by using the formula: DVA score ¼ abs½ðSVA log MAR 10Þ ½ðDVA log MAR 10Þ To establish the prevalence of decreased dynamic visual acuity the DVA score was calculated by determining the difference between the average of the two SVA trials and the average of the last two hDVA trials. A DVA score of more than two indicates gaze instability most likely due to a vestibular defect [23]. 2.3. Procedure Ethical clearance was granted by the Institution. The study was designed in accordance with the Declaration of Helsinki, 1964 [24]. In particular, the vulnerable status of children was recognized and respected at all times. 2.4. Data analysis SPSS Version 17, 20071 was used to do the statistical analysis of this study. Epi-Info Stat Calc Version 6 was used to calculate odds ratios and 95% confidence intervals. The one sided chi-square test or, if there were any cells with less than five, Fisher’s exact test, were used to test whether there was an association between SNHL and poor dynamic visual acuity. As the Shapiro–Wilk test indicated that the majority of M-ABC-2 data sets were not normally distributed, the Mann–Whitney U-test was used to analyze data in order to determine whether there was a significant difference in the ranking of the scores on the M-ABC-2 between children with SNHL and those with normal hearing. To establish the predictors of the M-ABC-2 total standard score, dummy variables were created for the presence of reduced DVA, the presence of SNHL and gender. These variables, with age in years included, were entered into a
Table 1 DVA score and degree of SNHL (N = 32). Degree of SNHL
DVA score
Total
2 (normal)
>2 (abnormal)
Profound 71+ dB Severe 51–70 dB Moderate 31–50 dB Slight 16–25 dB Within normal limits 0–15 dB
21 1 3 1 1
5 0 0 0 0
26 1 3 1 1
Total
27
5
32
forward stepwise regression model. This was followed by residual analysis. 3. Results The majority of children (26, 81.6%) in the group with SNHL were diagnosed with profound SNHL (Table 1). In the group with SNHL, 3 had bilateral cochlear implants, 13 had unilateral cochlear implants with a hearing aid in the opposite ear and 16 participants used bilateral hearing aids to address their hearing loss. Sign language is not utilized at the School. No child exhibited overt signs of significant loss of bilateral vestibular function. Of the participants with SNHL, 21 (65.6%) had reduced scores on the M-ABC-2 of which 18 were profoundly deaf. The participants with SNHL scored significantly lower than their normal-hearing counterparts on all the components of the M-ABC-2, with the greatest difference being in the balance component, followed by the overall score (Table 2 and Fig. 1). A total of five (15.6%) of the participants with SNHL had poor dynamic visual acuity. All the participants with an abnormal DVA score were diagnosed with profound SNHL (Table 1). In every case, the participants with SNHL and with an increased DVA score scored significantly less on all the components of the MABC-2 than the participants with SNHL and normal DVA scores. This difference was greatest in the balance component (Table 3 and Fig. 2). Age and dummy variables to represent gender, profound hearing impairment or less severe, presence of a cochlear implant and presence of an increased DVA score were included in the forward stepwise model. The variables retained by the forward stepwise model were the presence of an increased DVA score, age and presence of profound hearing loss. The adjusted r2 of this model was 0.33, which implies that 33% of the variance in the M-ABC-2 score could be attributed to the variables retained in the equation. There was one participant whose residual score was larger than two 2 standard residuals, and this participant was
Table 2 Comparison of the different components of the M-ABC-2 in the group with SNHL and the group with normal hearing (N = 64). Standard scores
Group
N
Mean rank
Sum of ranks
Mann–Whitney U
Z
p-Value
Total MABC
Normal hearing SNHL Total
32 32 64
43.55 21.45
1393.50 686.50
158.500
4.771
0.000
Manual dexterity
Normal hearing SNHL Total
32 32 64
38.38 26.63
1228.00 852.00
324.000
2.553
0.011
Aiming and catching
Normal hearing SNHL Total
32 32 64
38.92 26.08
1245.50 834.50
306.500
2.800
0.005
Balance
Normal hearing SNHL Total
32 32 64
44.11 20.89
1411.50 668.50
140.500
5.047
0.000
[(Fig._1)TD$IG]
[(Fig._2)TD$IG]
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Fig. 1. The mean scores of the different components of the MABC for the children with hearing loss (N = 32) and with normal hearing (N = 32).
Fig. 2. The mean scores of the different components of the MABC for the children with SNHL with normal DVA (N = 27) and with abnormal DVA (N = 5).
excluded from the analysis. The adjusted r2 of the final model was then 0.41, which implies that age, presence of a profound hearing loss and an increased DVA score collectively accounted for 41% of the variance. An abnormal DVA score reduced the M-ABC-2 score by 4.4 and profound hearing loss reduced the score by a further 3.0. In contrast, the performance was predicted to improve by 0.3 for each year of age (Table 4). No participants with normal hearing had reduced dynamic visual acuity or presented with a movement difficulty as measured by the M-ABC-2.
SNHL. Poor dynamic visual acuity associated with vestibular impairment has a major impact on the quality of life of adults; resulting in decreased levels of activity, difficulty with reading, avoidance of driving and limited social interactions [15,25]. Children with SNHL may present with poor dynamic visual acuity as a result of gaze instability due to reduced vestibular function. Results of the current study showed that participants with reduced dynamic visual acuity were all diagnosed with profound SNHL. Poor dynamic visual acuity can play a role in the child’s ability in learning to read, which may in turn result in learning difficulties and a consequent major impact on their education [14]. Children with poor dynamic visual acuity might have difficulties in taking part in sport and other recreational activities. Smooth pursuit eye movements are used to maintain moving targets on the fovea of the retina [26]. With deficits of the vestibular ocular reflex (VOR), the image of the moving target cannot stay on the fovea [26]. These children may have difficulty in following moving objects like a ball coming towards them. With gaze instability it is extremely difficult to follow a moving object with the eyes, especially when the child is running causing even more head movement. This can even be more challenging if the child has difficulty in maintaining balance as is suggested by the current study. This will be discussed in more detail below. It is suggested that routine screening for decreased dynamic visual acuity be included in the assessment of any child with SNHL. Gaze stability exercises have been used with great success in adults with poor dynamic visual acuity in the recovery of gaze stability [15]. Such therapy might have similar effects on children with poor dynamic visual acuity. This type of therapy falls within the scope of several health care professions and it is an available and feasible form of intervention in a developing country context.
4. Discussion One aim of the study was to establish the prevalence of impairments of motor performance and dynamic visual acuity in children with congenital and early acquired SNHL. Of the participants with SNHL, 65.6% had reduced scores on the MABC-2. A total of 15.6% of the participants with SNHL had poor dynamic visual acuity. A second aim was to determine the nature and extent of interaction between these parameters. The study showed that all participants with abnormal dynamic visual acuity also have reduced motor proficiency and that they were all profoundly deaf. This finding has major implications on the functioning and quality of life of these children. 4.1. Dynamic visual acuity It has been suggested that a difference of more than two lines on the DVA test is an indication of poor dynamic visual acuity due to reduced vestibular function [23]. No literature could be found on the prevalence of poor dynamic visual acuity in children with
Table 3 Comparison of the MABC-2 in children with SNHL with and without abnormal DVA (N = 32). Standard scores
DVA score
N
Mean
Standard deviation
Mean rank
Sum of ranks
Total MABC-2
Normal Abnormal Total
27 5 32
8.2 3.4
3 1.5
18.67 4.8
504 24
Manual dexterity
Normal Abnormal Total
27 5 32
8.9 5.6
2.5 2.1
18.2 7.3
Aiming and catching
Normal Abnormal Total
27 5 32
10.2 7
3.1 2.8
Balance
Normal Abnormal Total
27 5 32
7.4 2
3.9 1.2
Mann–Whitney U
Z
p-Value
9
3.052
0.002
491.5 36.5
21.5
2.41
0.016
17.91 8.9
483.5 44.5
29.5
1.99
0.047
18.61 5.1
502.5 25.5
10.5
2.978
0.003
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Table 4 Retained variables of the forward stepwise regression (N = 64). Unstandardized coefficients
Constant SNHL DVA score > 2 (Abn)
B
Std. error
11.44 3.32 4.72
0.39 0.59 1.01
T
Sig.
26.7 5.1 4.1
0.000 0.000 0.000
4.2. Motor impairment Participants with SNHL scored lower than their normal-hearing counterparts on all the components of the M-ABC-2, the greatest difference being in the balance component, followed by the total test score. The current study confirms findings of other studies that children with SNHL may have motor deficits and that balance is affected more than manual dexterity and ball skills in participants with SNHL [3–9,13]. Difficulties in maintaining balance can lead to challenges in normal childhood activities, such as playing on a jungle gym or riding a bicycle or a skateboard. Reduced ability to participate in normal play with other children may result in social isolation or even teasing or bullying. These issues with postural control are further compounded by the presence of disturbed DVA. Woollacott and Shumway-Cook [27] identified that the period between 4 and 6 years of age is critical for the development of postural control and it would therefore be important to evaluate the motor performance of children with SNHL to identify any delay of motor development as early as possible to allow for early referral for intervention. Aural rehabilitation is a must for children with SNHL – this study suggests that for a significant proportion of these children, there will be motor impairment, especially balance problems as well as reduced gaze stability that also need to be addressed as part of the overall rehabilitation program.
hearing loss to ensure that appropriate intervention is given in the case of poor motor performance. With increased age, central vestibular compensation is acquired due to the plasticity of the immature brain [2]. Visual and somatosensory systems compensate for the loss of vestibular function, and children with VH reach their motor developmental milestones by adolescence [2,13]. This could explain why participants with SNHL in the current study scored better on the M-ABC-2 with increased age. The only two variables retained by the forward stepwise model in predicting performance on the M-ABC-2, in the group with SNHL and in the normal-hearing group, were the presence of an increased DVA score and the presence of SNHL. As mentioned before, an increased DVA score is an indication of VH and more likely BVH [23]. This may be a confirmation that the DVA test is a reliable clinical test in predicting motor performance. 5. Conclusions The results of this study indicate that poor dynamic visual acuity is associated with SNHL in some participants. It is important to evaluate children with SNHL for the presence of a DVA abnormality as the latter can have serious implications for the safety, education and general well being of these children. Children with DVA abnormalities should be referred for appropriate therapy. Gaze stability exercises might be beneficial for children with poor dynamic visual acuity and could be the subject of future research. Even if the patient shows no overt vestibular deficit, therapists need to be cognizant that a vestibular component to the motor delay may exist, which might also need to be treated by adding VRT. Children with profound SNHL should be screened routinely for motor deficits because such children are at risk of having problems with motor performance, especially with balance. Problems with motor proficiency should be addressed by means of appropriate intervention to ensure optimal quality of life and a reduction of risks of accidents.
4.3. Association between impairments
5.1. Limitations of the study
Although no child demonstrated overt signs of VH the lack of clinical signs might be due to the compensation that can take place during childhood by using visual and somato-sensory systems [2,11]. In every case, the participants with SNHL and an increased DVA score scored less in every component of the M-ABC-2 than the participants with SNHL and normal DVA scores, with the greatest difference in the balance component. This finding suggests an association between dynamic visual acuity and motor performance. When a child has a decrease in dynamic visual acuity it has a negative influence on all the components of the M-ABC-2. The deficits in ball skills and manual dexterity appear to be due to the difficulty that the subjects had in stabilizing the image on the fovea while the head was moving. This may be as a result of a dysfunctional VOR. Difficulties in maintaining static and dynamic balance may be the result of a deficit in the VSR. It can therefore be argued that both decreased dynamic visual acuity and poor motor performance and particularly poor balance, are a result of reduced vestibular function.
Randomized sampling was not used to select participants but rather convenience sampling. The findings of this research can therefore not be generalized to the population with SNHL. There is also the possibility of sampling bias, whether consciously or unconsciously, because of the method of sampling. The selection of participants was done by an audiologist who knew the children and their histories. The study was done in an educational centre and therefore access to hospital and medical records was not possible and other conditions might have existed which were not reported by the parents and of which the audiologist was unaware.
4.4. Prediction of motor impairment As regression analysis identified SNHL and poor dynamic visual acuity as significant predictors of motor function, this indicates that motor performance is dependent on more than just the function of the semicircular canals. This might present a need for routine evaluation of the motor function of children with profound
5.2. Directions for further research As the majority of participants in the current study had congenital SNHL, further research is needed that will include more participants with acquired SNHL. The etiology of SNHL might have an influence on the prevalence of VH in children with SNHL. Further research is needed to determine whether vestibular rehabilitation therapy particularly gaze stability exercises, will improve the dynamic visual acuity and motor performance in children with SNHL. Gaze stability exercises could be included in parent guidance sessions. Parents can be taught to do these exercises with their children as a home program. This might be a feasible way to provide therapy to children with gaze instability, especially in developing countries with limited resources and service providers.
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Because no published South African studies could be found regarding the vestibular function of children with SNHL, more research is needed in this field in South Africa and other developing countries. It is possible that these results may differ from the results from developed countries due to the limited access to, as well as inadequate health care in developing countries. References [1] S. Angeli, Value of vestibular testing in young children with sensorineural hearing loss, Arch. Otolaryngol. Head Neck Surg. 129 (2003) 478–482. [2] K. Kaga, Vestibular compensation in infants and children with congenital and acquired vestibular loss in both ears, Int. J. Pediatr. Otorhinolaryngol. 49 (1999) 215–224. [3] T.K. Crowe, F.B. Horak, Motor proficiency associated with vestibular deficits in children with hearing impairments, Phys. Ther. 68 (1988) 1493–1499. [4] F.B. Horak, A. Shumway-Cook, T.K. Crowe, F.O. Black, Vestibular function and motor proficiency of children with impaired hearing, or with learning disability and motor impairments, Dev. Med. Child Neurol. 30 (1987) 64–79. [5] P.A. Selz, M. Girardi, H.R. Konrad, L.F. Hughes, Vestibular deficits in deaf children, Arch. Otolaryngol. Head Neck Surg. 115 (1996) 70–77. [6] S.L. Cushing, B.C. Papsin, J.A. Rutka, A.L. James, S.L. Blaser, K.A. Gordon, Vestibular end-organ and balance deficits after meningitis and cochlear implantation in children correlate poorly with functional outcome, Otol. Neurotol. 30 (4) (2009) 488–495. [7] S.L. Cushing, B.C. Papsin, J.A. Rutka, A.L. James, K.A. Gordon, Evidence of vestibular and balance dysfunction in children with profound sensorineural hearing loss using cochlear implants, Laryngoscope 118 (10) (2008) 1814–1823. [8] S.R. Wiener-Vacher, R. Obeid, M. Abou-Elew, Vestibular impairment after bacterial meningitis delays infant posturomotor development, J. Pediatr. (2012) (Epub ahead of print). [9] G. Zhou, M.A. Kenna, K. Stevens, G. Licameli, Assessment of vestibular function and balance dysfunction in children with profound sensorineural hearing loss using cochlear implants, Larynchoscope 118 (10) (2008) 1814–1823. [10] Z. Mehta, D.B. Stakiw, Childhood vestibular disorders: a tutorial, Commun. Dis. Q. 26 (2004) 5–16. [11] R. Nandi, L.M. Luxon, Development and assessment of the vestibular system, Int. J. Audiol. 47 (2008) 566–577.
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Motor proficiency and dynamic visual acuity in children with bilateral sensorineural hearing loss Willemien Martin a, Jennifer Jelsma b,*, Christine Rogers b a b
University of Cape Town, South Africa Department of Rehabilitation Sciences, University of Cape Town, South Africa
A R T I C L E I N F O
A B S T R A C T
Article history: Received 27 March 2012 Received in revised form 2 July 2012 Accepted 4 July 2012 Available online 22 July 2012
Aims and objectives: Due to the close relationship between the cochlea and the peripheral vestibular system, the function of the vestibular system may be impaired in children with sensorineural hearing loss. The aims of this study were to determine the prevalence of impairments of motor performance and dynamic visual acuity, and the nature and extent of interaction between these in children with sensorineural hearing loss between the ages of 4 and 14 years. Methods: This research utilized a correlational, cross-sectional, descriptive design. Thirty-two children with sensorineural hearing loss were matched according to age and gender with children with no hearing impairment. Motor performance was evaluated by means of the Movement Assessment Battery for Children-2 and dynamic visual acuity was evaluated with the dynamic visual acuity test. The performances of the two groups on the different tests were then compared. Data analysis: The one-sided chi-square test or Fisher’s exact test was used to determine whether there was any association between sensorineural hearing loss, impaired motor performance and poor dynamic visual acuity. The Mann–Whitney U-test was used to determine the difference between children with sensorineural hearing loss and those with normal hearing on the Movement Assessment Battery for Children-2. Forward stepwise regression was used to establish the predictors of the Movement Assessment Battery for Children-2 total standard score. The Kruskal–Wallis test was used to compare scores of children with normal hearing and those with a mild to moderate sensorineural hearing loss on the Movement Assessment Battery for Children-2. Results: Reduced dynamic visual acuity is associated with sensorineural hearing loss (p = 0.026). Motor performance is dependent on dynamic visual acuity and severity of sensorineural hearing loss (r2 = 0.41, p = 0.001). Conclusions: The results of this study indicate that in children with sensorineural hearing loss, the prevalence of reduced dynamic visual acuity is 15.6% and of motor impairment is 65.6%. Both abnormal dynamic visual acuity and motor impairment are associated with sensorineural hearing loss. It is important to evaluate children with sensorineural hearing loss for the presence of abnormal dynamic visual acuity as well as motor impairment, because it can have serious implications for the safety, education and general well being of these children. ß 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Children Dynamic visual acuity Motor performance Sensorineural hearing loss Vestibular hypofunction
1. Introduction Due to the close relationship between the cochlea and the peripheral vestibular system with respect to embryology, physiology and anatomy, the function of the vestibular system may be impaired in children with sensorineural hearing loss (SNHL) [1,2]. Several authors have shown that children with SNHL are more
* Corresponding author at: Faculty of Health Sciences, Anzio Road Observatory, 7925 Cape Town, South Africa. Tel.: +27 214066401. E-mail addresses: fi[email protected] (W. Martin), [email protected] (J. Jelsma), [email protected] (C. Rogers). 0165-5876/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2012.07.007
likely to have vestibular impairment than normal-hearing children [3–9]. Despite reports of vestibular disorders in children with SNHL, the functional integrity of the vestibular system is not often tested, and any impairment may therefore go undetected and untreated [10]. One reason might be that vestibular disorders are typically perceived as problems affecting mainly adults [10]. Another reason might be the difficulty describing the sensations of a vestibular disorder. It may be impossible for children, particularly young children, to describe what they experience. This can be due to a lack of basic communication skills, especially in children with hearing loss [10]. A third reason might be that compensation can take place during childhood by using visual and somatosensory systems [2,11]. In cases where impaired vestibular
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function was compensated for by other systems, vestibular hypofunction may be misdiagnosed or not identified because children demonstrate no outward abnormalities of gait and motor coordination [12]. The function of the mature vestibular system is to stabilize the position of the eyes, head and body in space, and to assist in maintaining an upright position [1,11]. The peripheral vestibular system consists of two parts with different functions. Firstly, the vestibular-ocular system is responsible for gaze stabilization and clear vision by means of the vestibular-ocular reflex (VOR). Secondly, the vestibular-spinal system as a result of the function of the vestibular-spinal reflex (VSR), contributes to muscle tone, aids in the acquisition of motor developmental milestones and it also helps with postural control [1]. Children with congenital vestibular abnormalities often display delayed gross motor development as well as problems with static and dynamic balance [1,13]. Late acquisition of developmental milestones in children with congenital vestibular dysfunction is thought to be the result of insufficient vestibular input [2]. However, age-expected motor proficiency is often achieved by adolescence as a result of compensation, especially when the visual and somato-sensory systems are intact [1–3]. Visual tasks, such as learning to read, may be problematic for children with congenital vestibular abnormalities due to impairment of the gaze stabilizing function of the vestibular system [14]. This may impact on scholastic performance, which in turn can lead to a reduced quality of life and sub-optimal levels of education [10]. Although there are indications that motor development and bilateral vestibular hypofunction (BVH) may be related, little research has been done on the relationship between BVH and dynamic visual acuity in children with congenital or early acquired SNHL [14]. BVH is defined as the loss of tonic and dynamic input from both labyrinths or from both vestibular nerves [2]. Dynamic visual acuity refers to the ability to see clearly while the head is moving [10]. In children with hearing loss, investigation of the impact of BVH on dynamic visual acuity and reading is important, because of the increased incidence of visual and reading problems in the hearing-impaired group [14]. It has been demonstrated that children with vestibular hypofunction (VH), particularly those with BVH, have poorer reading acuity scores than peers without VH regardless of hearing status [14]. Furthermore, reading acuity scores correlated with dynamic and not static visual acuity scores. This might be due to difficulties with visual stabilization [14]. The effect of BVH on dynamic visual acuity in children with congenital or early acquired SNHL has not been established conclusively. While there is some research on the reading acuity of children with vestibular hypofunction [14], there still remain some areas that could do with better delineation, such as the effect of poor dynamic visual acuity on motor performance of children. By comparing motor performance and dynamic visual acuity of hearing-impaired children with normal-hearing peers, it may be possible to determine whether impairment of these functions is associated with SNHL. Research in this field is important to determine the prevalence of impaired motor performance and reduced dynamic visual acuity in children with SNHL in order to provide healthcare professionals with the necessary information to address these possible impairments; for example, by highlighting the need for vestibular rehabilitation therapy, which is known to target gaze stabilization effectively in adults [15]. The aims of the study were therefore, in children with congenital and early acquired SNHL, to establish the prevalence of impairments of motor performance and dynamic visual acuity. A second aim was to determine the nature and extent of interaction between these parameters.
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1.1. Research setting The study took place at a school (the School) which offers education to typically developing children and children with SNHL. This mainstream school is regard to be unique in the world because of its specific curriculum as well as the inclusion of a few children with hearing loss and with no other disabilities into regular classes where they can learn alongside their peers with normal hearing. 2. Methodology The study utilized a correlational, cross-sectional, descriptive design. 2.1. Sample A sample of convenience was utilized as the cases included only those children attending the School with SNHL and as such was not representative of the population of children with SNHL. Parental reports of their child’s neurological problems, cochlear implants in the preceding 12 months, conductive hearing loss, poor visual acuity that was not correctable, taking medication with ocular, neuro-otological or vestibular side-effects and learning disabilities resulted in the child not being invited to participate in the study. As the study was school based, the researcher did not have access to the medical records of the children and had to rely on parental report of the medical history. The sample size was based on the need to ensure that the sample was large enough to perform multiple regression analysis. Using a statistical package [16] and data from a previous study, it was calculate that a total of 52 participants needed to enroll. A total of 64 participants took part in the current study which included all eligible children with SNHL from the School. The sample of children with SNHL comprised 32 participants of which 15 were female. The mean age of the children was 9.4 years (SD 2.4, range 4.5–13.2). There were 32 normalhearing children of which 17 were males. The mean age of the participants was 9.4 years (SD 2.5, range 4.6–13.3). An audiologist of the School who was familiar with the medical history of the children and who had access to their records, selected the children with SNHL and matched them with 32 normal-hearing children according to age and gender. 2.2. Instrumentation The classification system for hearing loss in children provided by Northern and Downs [17] was used to categorize the degree of hearing loss. A pediatric scale was developed due to the vastly different effect of hearing loss in children when compared to adults [17]. Movement ability was tested using the Movement Assessment Battery for Children-2 (MABC-2), which has been reported to be a reliable and valid test of motor performance in children [18–20]. The intra-class correlations (ICC) for inter-rater reliability for the M-ABC-2 exceeded 0.95 and ranged between 0.92 and 0.98 for the test–retest reliability [21]. It includes three different components: manual dexterity, ball skills and balance. Scores are calculated using each of these components and a standard score is derived. The total test score ranges between a minimum of one and a maximum of 19; with a score of eight or more indicating that no movement difficulty is present [22]. A standard score of six or seven suggests that the child is at risk of a movement difficulty and a standard score of five or less indicates a significant movement difficulty [23]. The dynamic visual acuity (DVA) test that was adapted by Rine and Braswell [23] for use with young children was utilized in the current study. The Lea vision chart which has symbols instead of
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letters was used. Rine and Braswell [23] found that the test–retest reliability for SVA and horizontal DVA was excellent with ICC = 0.94 and 0.84 respectively as well as the inter-rater reliability with ICC for SVA = 0.93 and for horizontal DVA = 0.88. Sensitivity, specificity as well as positive and negative predictive values for BVH were 100%, regardless of age (ANOVA p = 0.007) [23]. The participant began to identify symbols on the middle line (20/200). This was continued for successive lines until the participant missed three of the five optotypes on a line. The log MAR values of this line and those of the lowest line for which all the optotypes were correct were recorded [23]. This was done under two conditions: (1) head stationary, and (2) head tilted forward with the neck in 308 of flexion and manually rotated 308 by the researcher (sinusoidally, 158 from centre to the left and to the right), to the beat of a metronome at 2 Hz (hDVA). A dynamic visual acuity score was calculated as the difference between static visual acuity (SVA) and dynamic visual acuity (hDVA) in lines by using the formula: DVA score ¼ abs½ðSVA log MAR 10Þ ½ðDVA log MAR 10Þ To establish the prevalence of decreased dynamic visual acuity the DVA score was calculated by determining the difference between the average of the two SVA trials and the average of the last two hDVA trials. A DVA score of more than two indicates gaze instability most likely due to a vestibular defect [23]. 2.3. Procedure Ethical clearance was granted by the Institution. The study was designed in accordance with the Declaration of Helsinki, 1964 [24]. In particular, the vulnerable status of children was recognized and respected at all times. 2.4. Data analysis SPSS Version 17, 20071 was used to do the statistical analysis of this study. Epi-Info Stat Calc Version 6 was used to calculate odds ratios and 95% confidence intervals. The one sided chi-square test or, if there were any cells with less than five, Fisher’s exact test, were used to test whether there was an association between SNHL and poor dynamic visual acuity. As the Shapiro–Wilk test indicated that the majority of M-ABC-2 data sets were not normally distributed, the Mann–Whitney U-test was used to analyze data in order to determine whether there was a significant difference in the ranking of the scores on the M-ABC-2 between children with SNHL and those with normal hearing. To establish the predictors of the M-ABC-2 total standard score, dummy variables were created for the presence of reduced DVA, the presence of SNHL and gender. These variables, with age in years included, were entered into a
Table 1 DVA score and degree of SNHL (N = 32). Degree of SNHL
DVA score
Total
2 (normal)
>2 (abnormal)
Profound 71+ dB Severe 51–70 dB Moderate 31–50 dB Slight 16–25 dB Within normal limits 0–15 dB
21 1 3 1 1
5 0 0 0 0
26 1 3 1 1
Total
27
5
32
forward stepwise regression model. This was followed by residual analysis. 3. Results The majority of children (26, 81.6%) in the group with SNHL were diagnosed with profound SNHL (Table 1). In the group with SNHL, 3 had bilateral cochlear implants, 13 had unilateral cochlear implants with a hearing aid in the opposite ear and 16 participants used bilateral hearing aids to address their hearing loss. Sign language is not utilized at the School. No child exhibited overt signs of significant loss of bilateral vestibular function. Of the participants with SNHL, 21 (65.6%) had reduced scores on the M-ABC-2 of which 18 were profoundly deaf. The participants with SNHL scored significantly lower than their normal-hearing counterparts on all the components of the M-ABC-2, with the greatest difference being in the balance component, followed by the overall score (Table 2 and Fig. 1). A total of five (15.6%) of the participants with SNHL had poor dynamic visual acuity. All the participants with an abnormal DVA score were diagnosed with profound SNHL (Table 1). In every case, the participants with SNHL and with an increased DVA score scored significantly less on all the components of the MABC-2 than the participants with SNHL and normal DVA scores. This difference was greatest in the balance component (Table 3 and Fig. 2). Age and dummy variables to represent gender, profound hearing impairment or less severe, presence of a cochlear implant and presence of an increased DVA score were included in the forward stepwise model. The variables retained by the forward stepwise model were the presence of an increased DVA score, age and presence of profound hearing loss. The adjusted r2 of this model was 0.33, which implies that 33% of the variance in the M-ABC-2 score could be attributed to the variables retained in the equation. There was one participant whose residual score was larger than two 2 standard residuals, and this participant was
Table 2 Comparison of the different components of the M-ABC-2 in the group with SNHL and the group with normal hearing (N = 64). Standard scores
Group
N
Mean rank
Sum of ranks
Mann–Whitney U
Z
p-Value
Total MABC
Normal hearing SNHL Total
32 32 64
43.55 21.45
1393.50 686.50
158.500
4.771
0.000
Manual dexterity
Normal hearing SNHL Total
32 32 64
38.38 26.63
1228.00 852.00
324.000
2.553
0.011
Aiming and catching
Normal hearing SNHL Total
32 32 64
38.92 26.08
1245.50 834.50
306.500
2.800
0.005
Balance
Normal hearing SNHL Total
32 32 64
44.11 20.89
1411.50 668.50
140.500
5.047
0.000
[(Fig._1)TD$IG]
[(Fig._2)TD$IG]
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Fig. 1. The mean scores of the different components of the MABC for the children with hearing loss (N = 32) and with normal hearing (N = 32).
Fig. 2. The mean scores of the different components of the MABC for the children with SNHL with normal DVA (N = 27) and with abnormal DVA (N = 5).
excluded from the analysis. The adjusted r2 of the final model was then 0.41, which implies that age, presence of a profound hearing loss and an increased DVA score collectively accounted for 41% of the variance. An abnormal DVA score reduced the M-ABC-2 score by 4.4 and profound hearing loss reduced the score by a further 3.0. In contrast, the performance was predicted to improve by 0.3 for each year of age (Table 4). No participants with normal hearing had reduced dynamic visual acuity or presented with a movement difficulty as measured by the M-ABC-2.
SNHL. Poor dynamic visual acuity associated with vestibular impairment has a major impact on the quality of life of adults; resulting in decreased levels of activity, difficulty with reading, avoidance of driving and limited social interactions [15,25]. Children with SNHL may present with poor dynamic visual acuity as a result of gaze instability due to reduced vestibular function. Results of the current study showed that participants with reduced dynamic visual acuity were all diagnosed with profound SNHL. Poor dynamic visual acuity can play a role in the child’s ability in learning to read, which may in turn result in learning difficulties and a consequent major impact on their education [14]. Children with poor dynamic visual acuity might have difficulties in taking part in sport and other recreational activities. Smooth pursuit eye movements are used to maintain moving targets on the fovea of the retina [26]. With deficits of the vestibular ocular reflex (VOR), the image of the moving target cannot stay on the fovea [26]. These children may have difficulty in following moving objects like a ball coming towards them. With gaze instability it is extremely difficult to follow a moving object with the eyes, especially when the child is running causing even more head movement. This can even be more challenging if the child has difficulty in maintaining balance as is suggested by the current study. This will be discussed in more detail below. It is suggested that routine screening for decreased dynamic visual acuity be included in the assessment of any child with SNHL. Gaze stability exercises have been used with great success in adults with poor dynamic visual acuity in the recovery of gaze stability [15]. Such therapy might have similar effects on children with poor dynamic visual acuity. This type of therapy falls within the scope of several health care professions and it is an available and feasible form of intervention in a developing country context.
4. Discussion One aim of the study was to establish the prevalence of impairments of motor performance and dynamic visual acuity in children with congenital and early acquired SNHL. Of the participants with SNHL, 65.6% had reduced scores on the MABC-2. A total of 15.6% of the participants with SNHL had poor dynamic visual acuity. A second aim was to determine the nature and extent of interaction between these parameters. The study showed that all participants with abnormal dynamic visual acuity also have reduced motor proficiency and that they were all profoundly deaf. This finding has major implications on the functioning and quality of life of these children. 4.1. Dynamic visual acuity It has been suggested that a difference of more than two lines on the DVA test is an indication of poor dynamic visual acuity due to reduced vestibular function [23]. No literature could be found on the prevalence of poor dynamic visual acuity in children with
Table 3 Comparison of the MABC-2 in children with SNHL with and without abnormal DVA (N = 32). Standard scores
DVA score
N
Mean
Standard deviation
Mean rank
Sum of ranks
Total MABC-2
Normal Abnormal Total
27 5 32
8.2 3.4
3 1.5
18.67 4.8
504 24
Manual dexterity
Normal Abnormal Total
27 5 32
8.9 5.6
2.5 2.1
18.2 7.3
Aiming and catching
Normal Abnormal Total
27 5 32
10.2 7
3.1 2.8
Balance
Normal Abnormal Total
27 5 32
7.4 2
3.9 1.2
Mann–Whitney U
Z
p-Value
9
3.052
0.002
491.5 36.5
21.5
2.41
0.016
17.91 8.9
483.5 44.5
29.5
1.99
0.047
18.61 5.1
502.5 25.5
10.5
2.978
0.003
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Table 4 Retained variables of the forward stepwise regression (N = 64). Unstandardized coefficients
Constant SNHL DVA score > 2 (Abn)
B
Std. error
11.44 3.32 4.72
0.39 0.59 1.01
T
Sig.
26.7 5.1 4.1
0.000 0.000 0.000
4.2. Motor impairment Participants with SNHL scored lower than their normal-hearing counterparts on all the components of the M-ABC-2, the greatest difference being in the balance component, followed by the total test score. The current study confirms findings of other studies that children with SNHL may have motor deficits and that balance is affected more than manual dexterity and ball skills in participants with SNHL [3–9,13]. Difficulties in maintaining balance can lead to challenges in normal childhood activities, such as playing on a jungle gym or riding a bicycle or a skateboard. Reduced ability to participate in normal play with other children may result in social isolation or even teasing or bullying. These issues with postural control are further compounded by the presence of disturbed DVA. Woollacott and Shumway-Cook [27] identified that the period between 4 and 6 years of age is critical for the development of postural control and it would therefore be important to evaluate the motor performance of children with SNHL to identify any delay of motor development as early as possible to allow for early referral for intervention. Aural rehabilitation is a must for children with SNHL – this study suggests that for a significant proportion of these children, there will be motor impairment, especially balance problems as well as reduced gaze stability that also need to be addressed as part of the overall rehabilitation program.
hearing loss to ensure that appropriate intervention is given in the case of poor motor performance. With increased age, central vestibular compensation is acquired due to the plasticity of the immature brain [2]. Visual and somatosensory systems compensate for the loss of vestibular function, and children with VH reach their motor developmental milestones by adolescence [2,13]. This could explain why participants with SNHL in the current study scored better on the M-ABC-2 with increased age. The only two variables retained by the forward stepwise model in predicting performance on the M-ABC-2, in the group with SNHL and in the normal-hearing group, were the presence of an increased DVA score and the presence of SNHL. As mentioned before, an increased DVA score is an indication of VH and more likely BVH [23]. This may be a confirmation that the DVA test is a reliable clinical test in predicting motor performance. 5. Conclusions The results of this study indicate that poor dynamic visual acuity is associated with SNHL in some participants. It is important to evaluate children with SNHL for the presence of a DVA abnormality as the latter can have serious implications for the safety, education and general well being of these children. Children with DVA abnormalities should be referred for appropriate therapy. Gaze stability exercises might be beneficial for children with poor dynamic visual acuity and could be the subject of future research. Even if the patient shows no overt vestibular deficit, therapists need to be cognizant that a vestibular component to the motor delay may exist, which might also need to be treated by adding VRT. Children with profound SNHL should be screened routinely for motor deficits because such children are at risk of having problems with motor performance, especially with balance. Problems with motor proficiency should be addressed by means of appropriate intervention to ensure optimal quality of life and a reduction of risks of accidents.
4.3. Association between impairments
5.1. Limitations of the study
Although no child demonstrated overt signs of VH the lack of clinical signs might be due to the compensation that can take place during childhood by using visual and somato-sensory systems [2,11]. In every case, the participants with SNHL and an increased DVA score scored less in every component of the M-ABC-2 than the participants with SNHL and normal DVA scores, with the greatest difference in the balance component. This finding suggests an association between dynamic visual acuity and motor performance. When a child has a decrease in dynamic visual acuity it has a negative influence on all the components of the M-ABC-2. The deficits in ball skills and manual dexterity appear to be due to the difficulty that the subjects had in stabilizing the image on the fovea while the head was moving. This may be as a result of a dysfunctional VOR. Difficulties in maintaining static and dynamic balance may be the result of a deficit in the VSR. It can therefore be argued that both decreased dynamic visual acuity and poor motor performance and particularly poor balance, are a result of reduced vestibular function.
Randomized sampling was not used to select participants but rather convenience sampling. The findings of this research can therefore not be generalized to the population with SNHL. There is also the possibility of sampling bias, whether consciously or unconsciously, because of the method of sampling. The selection of participants was done by an audiologist who knew the children and their histories. The study was done in an educational centre and therefore access to hospital and medical records was not possible and other conditions might have existed which were not reported by the parents and of which the audiologist was unaware.
4.4. Prediction of motor impairment As regression analysis identified SNHL and poor dynamic visual acuity as significant predictors of motor function, this indicates that motor performance is dependent on more than just the function of the semicircular canals. This might present a need for routine evaluation of the motor function of children with profound
5.2. Directions for further research As the majority of participants in the current study had congenital SNHL, further research is needed that will include more participants with acquired SNHL. The etiology of SNHL might have an influence on the prevalence of VH in children with SNHL. Further research is needed to determine whether vestibular rehabilitation therapy particularly gaze stability exercises, will improve the dynamic visual acuity and motor performance in children with SNHL. Gaze stability exercises could be included in parent guidance sessions. Parents can be taught to do these exercises with their children as a home program. This might be a feasible way to provide therapy to children with gaze instability, especially in developing countries with limited resources and service providers.
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Because no published South African studies could be found regarding the vestibular function of children with SNHL, more research is needed in this field in South Africa and other developing countries. It is possible that these results may differ from the results from developed countries due to the limited access to, as well as inadequate health care in developing countries. References [1] S. Angeli, Value of vestibular testing in young children with sensorineural hearing loss, Arch. Otolaryngol. Head Neck Surg. 129 (2003) 478–482. [2] K. Kaga, Vestibular compensation in infants and children with congenital and acquired vestibular loss in both ears, Int. J. Pediatr. Otorhinolaryngol. 49 (1999) 215–224. [3] T.K. Crowe, F.B. Horak, Motor proficiency associated with vestibular deficits in children with hearing impairments, Phys. Ther. 68 (1988) 1493–1499. [4] F.B. Horak, A. Shumway-Cook, T.K. Crowe, F.O. Black, Vestibular function and motor proficiency of children with impaired hearing, or with learning disability and motor impairments, Dev. Med. Child Neurol. 30 (1987) 64–79. [5] P.A. Selz, M. Girardi, H.R. Konrad, L.F. Hughes, Vestibular deficits in deaf children, Arch. Otolaryngol. Head Neck Surg. 115 (1996) 70–77. [6] S.L. Cushing, B.C. Papsin, J.A. Rutka, A.L. James, S.L. Blaser, K.A. Gordon, Vestibular end-organ and balance deficits after meningitis and cochlear implantation in children correlate poorly with functional outcome, Otol. Neurotol. 30 (4) (2009) 488–495. [7] S.L. Cushing, B.C. Papsin, J.A. Rutka, A.L. James, K.A. Gordon, Evidence of vestibular and balance dysfunction in children with profound sensorineural hearing loss using cochlear implants, Laryngoscope 118 (10) (2008) 1814–1823. [8] S.R. Wiener-Vacher, R. Obeid, M. Abou-Elew, Vestibular impairment after bacterial meningitis delays infant posturomotor development, J. Pediatr. (2012) (Epub ahead of print). [9] G. Zhou, M.A. Kenna, K. Stevens, G. Licameli, Assessment of vestibular function and balance dysfunction in children with profound sensorineural hearing loss using cochlear implants, Larynchoscope 118 (10) (2008) 1814–1823. [10] Z. Mehta, D.B. Stakiw, Childhood vestibular disorders: a tutorial, Commun. Dis. Q. 26 (2004) 5–16. [11] R. Nandi, L.M. Luxon, Development and assessment of the vestibular system, Int. J. Audiol. 47 (2008) 566–577.
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