Research in Developmental Disabilities 35 (2014) 2728–2734
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Research in Developmental Disabilities
Balance assessment in hearing-impaired children Katarzyna Walicka-Cuprys´ a, Łukasz Przygoda a, Ewelina Czenczek a,b,c, Aleksandra Truszczyn´ska b,*, Justyna Drzał-Grabiec a, Trzaskoma Zbigniew b, Adam Tarnowski a,b,c a
Institute of Physiotherapy, University of Rzeszo´w, Warszawska 26a, Poland Faculty of Rehabilitation, Jo´zef Piłsudski University of Physical Education in Warsaw, Marymoncka St. 34, 00-968 Warsaw, Poland c Military Institute of Aviation Medicine, Krasin´skiego 54, 01-755 Warsaw, Poland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 April 2014 Received in revised form 26 June 2014 Accepted 2 July 2014 Available online 30 July 2014
According to the scientific reports the postural stability is inseparably associated with hearing organ’s correct functioning. The aim of the study was to evaluate the degree of disorders occurring in balance reactions in this group of children with profound hearing loss compared to their healthy peers. The study worked with a total of 228 children, including 65 who are deaf (DCH) and 163 subjects without any hearing deficits (CON) in the control group. Stabilometric measurements were performed with the use of a force distribution platform. The results indicate statistically significant differences in terms of one parameter (the total path length) recorded in the test with the eyes open and a whole range of parameters recorded when the subjects had their eyes closed (the width, height, and area of the ellipse, the total path length, and the horizontal and vertical sway). The study results showed better values of the static balance parameters in deaf children as compared to their peers without hearing disorders and the differences were particularly evident in the test with the subject’s eyes closed. The results suggest significantly better processing of sensory stimuli in postural reactions particularly from propioception, and to a lesser extent, from the vision system observed in the subjects as compared to their peers in the control group. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Balance Children Early intervention Hearing impairment Postural control Sensory deprivation
1. Introduction The development of normal postural reactions that oppose the force of gravity and maintain the body’s balance during exercise and rest is possible due to stimulation of the labyrinth and the labyrinth’s cooperation with proprioception, vision, touch, and hearing (Nakajima, Kaga, Takekoshi, & Sakuraba, 2012). Vestibular receptors receive impulses related to the position of the head in space and generate reflexes that play a key role in basic motor responses; for example maintaining head and body posture. Due to this complex process, we have, inter alia, a sense of control over the moving body and its orientation in space (Greenwald & Gurley, 2013). Hearing-related organs develop with and work in close cooperation with the vestibular system. The receptors of both systems are located in the inner ear, from which information is transmitted to
* Corresponding author. Tel.: +48 22 834 17 77; fax: +48 22 834 17 77. E-mail addresses: [email protected] (K. Walicka-Cuprys´), [email protected] (Ł. Przygoda), [email protected] (E. Czenczek), [email protected] (A. Truszczyn´ska), [email protected] (J. Drzał-Grabiec), [email protected] (T. Zbigniew), [email protected] (A. Tarnowski). http://dx.doi.org/10.1016/j.ridd.2014.07.008 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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the brainstem through cranial nerve VIII. The close neuro-anatomical relationship of these systems results in a situation in which damage to the cochlea, semicircular canals, or both, leads to vestibular dysfunction, which may be related to conditions such as balance impairment (Martin, Jelsma, & Rogers, 2012; Schwab & Kontorinis, 2011). According to the available data, as many as 30 to 85% of children with severe or profound hearing loss have some degree of vestibular deficit (De Kegel et al., 2010; Del Pino, Femia, & Pe´rez-Ferna´ndezc, 2011), which in turn interferes with the many areas of the children’s development, including static and dynamic balance reactions, coordination, and the speed of performed movements (Chilosi et al., 2010). In children, balance is inextricably linked to the mastering of basic motor skills (Fisher et al., 2005). Shah, Rao, Malawade, and Khatri (2013) reported that children with hearing impairments have balance and motor deficits that are primarily due to concomitant damage to the vestibular structures. In most hearing-impaired children, fundamental motor skills, such as the maintenance of head, sitting, and bipedal positions, develop much more slowly than in children with normal hearing (Rajendran and Finita, 2010). To master these skills, a properly developed body schema that is based on perception and experience is essential. Sensations from the skin, proprioceptive information from the muscles and joints, and motion- and gravity-related information from the vestibular system are organized, integrated, and ultimately applied during daily activities. Due to the well-organized perceptions of the body, an individual can feel the actions of any given part of the body, how those parts move, and where those parts are in space. However, when the supply of information from one of the sensory systems is limited, for example, due to the loss of hearing, the feeling of one’s body within space may be affected, and result in a reduction of the maturity level of posture control (An, Yi, Jeon, & Park, 2009). Such reduced maturity levels can be particularly dangerous when the flow of information from another system, such as the visual system, is obstructed (e.g., when walking in the dark or riding a bicycle at dusk). Simultaneously, the poor postural control abilities of the deaf during childhood do not necessarily entail difficulties in the performance of everyday activities during adulthood (Kaga, 1999). Postural reactions may be well-developed in adolescence despite irregularities in the impulses received from the vestibular system due to the compensatory responses of the other systems. Therefore, it is important to examine the severities of the disorders of balance reactions that occur in hearing-impaired children and how such severities depend on the flow of information from other systems. Such evaluations may facilitate the decision to introduce measures to stimulate the relevant sensory systems as early as possible. 2. Objectives The aim of this study was to evaluate the severities of the disorders of balance reactions that occur in a group of children with profound hearing loss relative to children with normal hearing. 3. Methods 3.1. Participants The study examined a total of 228 children, including 65 subjects who were deaf (DCH) aged between 8 and 17, and a control group of 163 subjects without any hearing deficits aged between 8 and 16 (CON) (Table 1). This study was conducted in four schools in Rzeszo´w and two schools for hearing-impaired children in the Subcarpathian region of Poland. The 25 (38.46%) of participants with hearing loss been hearing impaired since birth, and 40 (61.54%) had hearing disorders acquired later. The general criterion for inclusion in this study was the lack of neurological and orthopedic disorders. Additional inclusion criteria were, for the study group, a degree of deafness 90 dB and, for the control group, a complete lack of hearing deficits. Exclusion criteria included: an intellectual disability and comorbid illnesses. This study was approved by the local Bioethical Committee and performed after obtaining written consent from the children’s parents. 3.2. Procedure First, the parents of the children completed a questionnaire. The following information was acquired via questionnaire filled by parents: date of birth, illness, and degree of deafness. In the second part of the study, stabilometric measurements Table 1 Characteristics of the subjects.
Number of subjects Sex Male Female Age [mean SD]
Hearing-impaired children
Children with normal hearing
65
163
46 19 13.4 (2.4)
79 84 11.9 (2.2)
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were performed with a force distribution platform that was produced by Zebris WinPDMS. Sign language was used to communicate with the deaf children. Static standing position with eyes open and then closed was tested (Giagazoglou et al., 2013; Haidan et al., 2008; Harringe et al., 2008). The subjects were instructed to maintain an upright position with their arms at their sides and their eyes fixed on a black point located 1.5 meters away while standing barefoot on the platform. The position of the black point was adjusted to for the heights and eye levels of the subjects. As previous studies (Ruhe, Fejer, & Walker, 2010; Scoppa, Capra, Gallamini, & Shiffer, 2013) have not provided clear guidelines concerning foot positions, the subjects were instructed to place their feet along the designated lines on the platform while maintaining a relaxed, natural position in which their feet were no more than hip-width apart. Simultaneously, the subjects were asked to refrain from shaking their heads, moving their arms, or turning during the test. To minimize any external effects, the tests were performed in a quiet room in which only the person being examined was present. The tests lasted 30 s, of which 20 s were recorded (Di Nardi, 2010). The first 10 s were spent preparing for the examination to eliminate uncontrolled center of pressure (COP) movements (Derlich, Kre˛cisz, & Kuczyn´ski, 2011). According to a typical procedure that has been utilized in similar studies, each participant performed 3 trials (Ruhe et al., 2010) for each of two tests. 3.3. Data analysis Static balance testing was performed on a Zebris WinPDMS platform, which measures the pressure distribution of static forces. The WinPDMS system analyses the statical pressure distribution in real-time. The platform has dimensions 600 mm 380 mm 20.1 mm (B H T) and 1536 pressure sensors with pressure measurement ranges 1–120 N/cm2 and a resolution of 1 sensor/cm2 sensor area 320 mm 480 mm. The sensors respond to load changes of the lower limbs. The testing was performed while data were recorded at the recommended sampling frequency of 20 Hz (Słomka, Juras, Sobota, & Bacik, 2013). Following registration, the system automatically performed basic analyses of the captured signals for stabilometric assessment. Multiple COP deflection during the test are marked with lines that create a different size elipse. The ellipse includes 95% of the COP. Characteristics of the circle are displayed in a chart. Balance was evaluated based on the average results obtained across the three trials (Ruhe et al., 2010) based on the following parameters: left leg COP in the front (LLF – mm), left leg COP in the back (LLB – mm), whole left leg COP (LLW – mm), right leg COP in the front (RLF – mm), right leg COP in the back (RLB – mm), whole right leg COP (RLW – mm), the width of the ellipse delineated by the COP (WE – mm), the height of the ellipse delineated by the COP (HE – mm), the angle of the ellipse delineated by the COP indicates the orientation of the direction of the longitudinal axis of the ellipse compared to the longitudinal (x-) axis of the platform in degree and the orientation direction (left or right) (AE – deg), the area of the ellipse (ARE – mm2), the total path length of the COP (TPL – mm), the horizontal sway of the COP (HS – mm), and the vertical sway of the COP (VS – mm). 3.4. Analysis Independent assessments were performed for each group. The normalities of the posturographic parameter distributions were examined with the Kolmogorov–Smirnov test. The analysis revealed that, of the 52 total analyses, the data from 24 were not normally distributed; thus, we decided to perform all analyses using nonparametric methods to harmonize the statistical results. In addition to the mean values, the medians were used for statistical description (because the median is a more reliable indicator of the characteristics of a non-normally distributed parameter). Comparisons between groups were performed using the Mann–Whitney U test for independent samples. 4. Results The results revealed statistically significant differences between the groups in terms of one parameter (i.e., total path length of the COP – TPL) that was recorded during the open-eye test (Table 2) and many parameters that were recorded during the closed-eye test (Table 3). The results from the hearing-impaired children during the eye-closed test were lower, (i.e., better) than those children from control group during the eye-open test, particularly in terms of the area (ARE), width (WE) and height (HE) of the ellipse that was delineated by the COP. The results from the children with normal hearing were similar across the two tests. Our analyses revealed that the hearing-impaired children exhibited lower (i.e., better) static balance parameters than did their normal hearing peers and that these differences were particularly evident in the closedeye test. Mann–Whitney U tests revealed significant differences in the total path lengths of the COPs (TPLs) in both tests (i.e., the open- and closed-eye tests). Additionally, in the open-eye test, the hearing-impaired children exhibited significantly lower values than did the children with normal hearing in the parameters of the area (ARE), width (WE) and height (HE) of the ellipse delineated by the COP and in the parameters of horizontal and vertical sway of the COP (HS and VS, respectively) (Table 3). 5. Discussion Hearing loss affects between 1 to 6 of every 1000 children worldwide, and among the affected children, 10% have profound hearing deficits (Rajendran & Roy, 2011). Due to the close relationship between the auditory and vestibular
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Table 2 Comparison of posturographic parameters recorded for the hearing-impaired and children with normal hearing children in the open-eye test. Parameter
1 2 3 4 5 6 7 8 9 10 11 12 13
LLF [mm] LLB [mm] LLW [mm] RLF [mm] RLB [mm] RLW [mm] WE [mm] HE [mm] AE [deg] ARE [mm2] TPL [mm] HS [mm] VS [mm]
Hearing-impaired children
Children with normal hearing
Mean
Median
Mean
Median
34.2 67.0 49.6 37.3 62.8 48.8 6.7 13.7 26.0 99.4 527.9* 3.6 4.9
33.1 69.5 49.3 35.7 63.6 50.4 5.5 10.0 16.8 43.3 496.5 2.7 3.9
31.6 68.4 50.2 33.6 66.4 49.8 6.7 13.5 28.4 78.5 1083.6 3.5 4.9
30.4 69.6 50.2 32.4 67.6 49.8 6.2 12.0 21.9 59.7 1059.3 3.2 4.4
Mann–Whitney U test
Significance level
4798.50 4967.00 4883.50 4545.50 4524.50 5115.00 4569.00 4449.00 4958.50 4484.00 664.00 4650.50 4598.00
.267 .462 .357 .094 .086 .685 .105 .059 .451 .070 .000 .150 .120
Parameters: left leg COP in the front (LLF), left leg COP in the back (LLB), whole left leg COP (LLW), right leg COP in the front (RLF), right leg COP in the back (RLB), whole right leg COP (RLW), width of the ellipse delineated by the COP (WE), height of the ellipse delineated by the COP (HE), angle of the ellipse with respect to the horizontal level (AE), area of the ellipse (ARE), total path length of the COP (TPL), horizontal sway of the COP (HS), and vertical sway of the COP (VS). * Statistically significance difference between the hearing-impaired and children with normal hearing (P 0.001).
Table 3 Comparison of the posturographic parameters recorded from the hearing-impaired and children with normal hearing in the closed-eye test. Parameter
1 2 3 4 5 6 7 8 9 10 11 12 13
LLF [mm] LLB [mm] LLW [mm] RLF [mm] RLB [mm] RLW [mm] WE [mm] HE [mm] AE [deg] ARE [mm2] TPL [mm] HS [mm] VS [mm]
Hearing-impaired children
Children with normal hearing
Mean
Median
Mean
Median
33.2 67.3 49.8 36.4 63.6 49.9 6.0* 12.6* 27.8 80.0* 529.6* 3.13** 4.69*
30.5 69.8 49.5 31.7 68.3 50.3 4.7 10.2 18.4 40.0 499.2 2.60 3.80
31.8 68.2 49.6 33.6 66.4 50.4 7.5 14.8 21.0 107.6 1108.4 3.56 5.72
29.7 70.3 49.4 32.5 67.5 50.6 6.5 13.7 12.9 70.2 1061.6 3.00 5.20
Mann–Whitney U test
Significance level
4892.50 5003.00 5205.50 4803.00 4823.50 5162.50 3749.00 3557.00 4534.00 3580.00 482.00 4111.00 3422.50
.368 .512 .838 .271 .292 .764 .001 .000 .090 .000 .000 .008 .000
Parameters: see the legend for Table 2. * P 0.001 for the differences between the hearing-impaired and children with normal hearing. ** P 0.01 for the differences between the hearing-impaired and children with normal hearing.
systems, it can be assumed that deaf children are at risk for deficits in body balance (Cushing, Papsin, Rutka, James, & Gordon, 2008). Balance reactions are responses to integrated stimuli that are delivered by proprioceptive and exteroceptive sensations, telereceptors, and the vestibular system; therefore, disorders in the reception of these stimuli from any of these receptors or systems can result in impaired stability (Sousa, Franca Bartos, & de Sousa Neto, 2012). The tests that are used in studies that assess balance function include static tests (i.e., the fulcrum of the body is fixed) and dynamic tests (i.e., the fulcrum of the body changes). The most well-known tests comprise a traditional test that involves standing on one leg, Romberg’s test, the Berg Balance Scale, the Fullerton Advanced Balance (FAB) test, and the Scale and Tapping test (i.e., the Fleishman test). More accurate and reliable diagnostic methods for the analysis of the static balance of hearing-impaired children, like those used in the current study, involve computer graphic records of shifts in the center of gravity that are via stabilometric platforms (the so-called posturographic tests) (Kostiukow, Rostkowska, & Samborski, 2009). The current results suggest that the processing of sensory stimuli during postural reactions, particularly stimuli from propioception and to a lesser extent from the visual system, was significantly better in the hearing-impaired subjects than in the control group. These finding agree with the ‘‘sensory compensation’’ hypothesis, which states that the loss of one sensory modality induces compensations in the other intact sensory modalities (Lo´pez-Crespo, Daza, & Me`ndez-Lo´pez, 2012). Our results can be explained by the fact that visual orienting is not essential for the maintenance of postural
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stability during static, quiet standing (Westcott, Lowes, & Richardson, 1997). Postural reactions are also based on information from the proprioceptors and the vestibular system (i.e., somatosensory and vestibular inputs). Only the integration of information that is received from the so-called active sensory channels affects the final postural response (Szymczyk, Druz˙bicki, Dudek, Szczepanik, & Snela, 2012). The results of this study may explain the reports of other authors who have confirmed that the most important information for maintaining balance in the upright position, even when the support surface is distorted, is the information from the proprioreceptors (Shumway-Cook & Woollacott, 2006). In contrast, visual stimuli are used in more difficult balance situations (Sundermier, Woollacott, Jensen, & Moore, 1996), and, in such situations, the vestibular system has a lesser role than does the sensory information (Dietz, Schubert, Discher, & Trippel, 1994). Findings similar to ours were reported by Wierzbicka-Damska, Samołyk, Jethon, Wiercin´ska, and Murawska-Ciałowicz (2005) who examined 29 hearing-impaired children and 38 hearing children aged 10–16 years on a stabilometric platform and observed superior better stabilometric values among the children with impaired hearing. The same conclusion has been reached by the authors of other studies (Kaga, 1999; An et al., 2009) who have suggested that children with hearing loss can manifest relatively normal postural reactions due to the adaptations afforded by sensory compensation. Moreover, the results of clinical balance tests that were conducted by De Kegel et al. (2011) revealed excellent overall test–retest reliabilities (ICCs above 0.80) in children with normal hearing and hearing-impaired children (ICCs above 0.90). Similar to the results of our study, in this aforementioned study, the area of the ellipse delineated by the COP was nearly two-fold lower in the hearing-impaired children than in the typically developing children. It means that hearing impaired children had two times better results of this stabilometric test, their COP inclination was smaller. However, in another study (De Kegel, Maes, Baetens, Dhooge, & Van Waelvelde, 2012), these same authors concluded that hearing-impaired children are at risk for balance deficits. Some authors have indicated that static balance reactions in children with profound hearing loss can be weakened. Similar studies were conducted by Jernice et al. (2011). Authors have suggested that the parameters of children with hearing-impairments during static tests of standing on one leg with the open and closed eyes are lower than those of health controls. The higher mean path length (MPL) and root mean square (RMS) value were recorded in the anterior–posterior plane (AP) and the medial–lateral plane (ML) confirm the weaker balance capabilities of hearing-impaired children. Nevertheless, the analyses of these research materials revealed that these results were not confirmed in a larger sample of subjects (Tan, Nonis, & Chow, 2011). Similar conclusions have been presented by researchers from Iran who found that, in a group of 30 children with profound hearing loss, 16.7–100% of the children were characterized by the incorrect execution of a balance task over seven trials (Jafari, Malayeri, Rezazadeh, Haji, & Heydari, 2011). The majority of reports of research on the dynamic balance of children with hearing impairments indicate reduced functionality (Rahman, 2005). The study conducted by Wong, Leung, Poon, Leung, & Lau (2013) showed that children with severe-to-profound-grade hearing impairments exhibited balance deficits as assessed with the Bruininkse–Oseretsky test of Motor Proficiency (BOT2), the Pediatric Functional Reach Test (FRT), the Pediatric Version of the Clinical Test for Sensory Interaction of Balance (P-CTSIB) and the Test of Postrotary Nystagmus (PRN). The present results and the results of other authors do not unequivocally prove that children with hearing impairment have significantly worse postural stabilities than do their hearing peers. Further research in this area is necessary to obtain definite conclusions.
6. Limitations We acknowledge some limitations in this study. One of the most relevant limitations is the lack of a standard, reliable, validated outcome measure for the assessment of static balance in children. The balance parameters and their modified versions that were used in this work have been widely used to assess people with normal hearing and patients with different illnesses. Other limitations of our study include the difference in the numbers of hearing impaired and children with normal hearing and the fact that we used a single observation of the children’s static balance. Similar differences in the numbers of typically developing and hearing impaired children were present in other studies; for example, in the study conducted by De Kegel et al. (2011), the ratio of typically developing to hearing impaired children was 2.1–1.0. The main reason for this problem is probably related to the presence of numerous significant inter-population differences. We plan conduct further assessments in this area utilizing equal numbers of hearing-impaired and children with normal hearing and repeated measurements. Additionally, it will be important to perform measurements of dynamic equilibrium in groups of hearing-impaired children to determine the correlations between the recorded parameters and the degree of hearing loss. The lack of a comparison between the static and dynamic measures of postural stability in this current study precludes the identification of (1) differential responses between the hearing-impaired and children with normal hearing for the maintenance of postural stability and (2) the different stresses on the systems that are necessary for the maintenance of postural stability under different dynamic conditions. Some authors have concluded that dynamic measures of postural stability are more difficult to obtain but are also more informative. Lastly, in the present study, we were unable to examine whether gender differences may have influenced postural stability.
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7. Conclusions The results of the present study revealed that the hearing-impaired children exhibited superior static balance parameter values than did their children with normal hearing peers and that these differences were particularly evident in the closedeye test. Our results suggest that the hearing-impaired children exhibited significantly better processing of sensory stimuli in postural reactions, particularly proprioception stimuli and to a lesser extent visual stimuli, than did their peers in the control group. References An, M. H., Yi, C. H., Jeon, H. S., & Park, S. Y. (2009). Age-related changes of single-limb standing balance in children with and without deafness. International Journal of Pediatric Otorhinolaryngology, 73, 1539–1544. Chilosi, A. M., Comparini, A., Scusa, M. F., Berrettini, S., Forli, F., Battini, R., et al. (2010). Neurodevelopmental disorders in children with severe to profound sensorineural hearing loss: A clinical study. 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Tan, J., Nonis, K., & Chow, J. (2011). The balance control of children with and without hearing impairment in Singapore – A case study. International Journal of Special Education, 26(3), 260–275. Westcott, S. L., Lowes, L. P., & Richardson, P. K. (1997). Evaluation of postural stability in children: Current theories and assessment tools. Physical Therapy, 77(6), 629–645. Wierzbicka-Damska, I., Samołyk, A., Jethon, Z., Wiercin´ska, J., & Murawska-Ciałowicz, E. (2005). Physical efficiency of 10–16-year-old boys with hearing impairment. Roczniki Akademii Medycznej W Bialymstoku, 50(Suppl. 1), 167–169. Wong, T. P. S., Leung, E. Y. W., Poon, C. Y. C., Leung, C. Y. F., & Lau, B. P. H. (2013). Balance performance in children with unilateral and bilateral severe-to-profoundgrade hearing impairment. Hong Kong Physiotherapy Journal, 31, 81–87.
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Balance assessment in hearing-impaired children Katarzyna Walicka-Cuprys´ a, Łukasz Przygoda a, Ewelina Czenczek a,b,c, Aleksandra Truszczyn´ska b,*, Justyna Drzał-Grabiec a, Trzaskoma Zbigniew b, Adam Tarnowski a,b,c a
Institute of Physiotherapy, University of Rzeszo´w, Warszawska 26a, Poland Faculty of Rehabilitation, Jo´zef Piłsudski University of Physical Education in Warsaw, Marymoncka St. 34, 00-968 Warsaw, Poland c Military Institute of Aviation Medicine, Krasin´skiego 54, 01-755 Warsaw, Poland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 April 2014 Received in revised form 26 June 2014 Accepted 2 July 2014 Available online 30 July 2014
According to the scientific reports the postural stability is inseparably associated with hearing organ’s correct functioning. The aim of the study was to evaluate the degree of disorders occurring in balance reactions in this group of children with profound hearing loss compared to their healthy peers. The study worked with a total of 228 children, including 65 who are deaf (DCH) and 163 subjects without any hearing deficits (CON) in the control group. Stabilometric measurements were performed with the use of a force distribution platform. The results indicate statistically significant differences in terms of one parameter (the total path length) recorded in the test with the eyes open and a whole range of parameters recorded when the subjects had their eyes closed (the width, height, and area of the ellipse, the total path length, and the horizontal and vertical sway). The study results showed better values of the static balance parameters in deaf children as compared to their peers without hearing disorders and the differences were particularly evident in the test with the subject’s eyes closed. The results suggest significantly better processing of sensory stimuli in postural reactions particularly from propioception, and to a lesser extent, from the vision system observed in the subjects as compared to their peers in the control group. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Balance Children Early intervention Hearing impairment Postural control Sensory deprivation
1. Introduction The development of normal postural reactions that oppose the force of gravity and maintain the body’s balance during exercise and rest is possible due to stimulation of the labyrinth and the labyrinth’s cooperation with proprioception, vision, touch, and hearing (Nakajima, Kaga, Takekoshi, & Sakuraba, 2012). Vestibular receptors receive impulses related to the position of the head in space and generate reflexes that play a key role in basic motor responses; for example maintaining head and body posture. Due to this complex process, we have, inter alia, a sense of control over the moving body and its orientation in space (Greenwald & Gurley, 2013). Hearing-related organs develop with and work in close cooperation with the vestibular system. The receptors of both systems are located in the inner ear, from which information is transmitted to
* Corresponding author. Tel.: +48 22 834 17 77; fax: +48 22 834 17 77. E-mail addresses: [email protected] (K. Walicka-Cuprys´), [email protected] (Ł. Przygoda), [email protected] (E. Czenczek), [email protected] (A. Truszczyn´ska), [email protected] (J. Drzał-Grabiec), [email protected] (T. Zbigniew), [email protected] (A. Tarnowski). http://dx.doi.org/10.1016/j.ridd.2014.07.008 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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the brainstem through cranial nerve VIII. The close neuro-anatomical relationship of these systems results in a situation in which damage to the cochlea, semicircular canals, or both, leads to vestibular dysfunction, which may be related to conditions such as balance impairment (Martin, Jelsma, & Rogers, 2012; Schwab & Kontorinis, 2011). According to the available data, as many as 30 to 85% of children with severe or profound hearing loss have some degree of vestibular deficit (De Kegel et al., 2010; Del Pino, Femia, & Pe´rez-Ferna´ndezc, 2011), which in turn interferes with the many areas of the children’s development, including static and dynamic balance reactions, coordination, and the speed of performed movements (Chilosi et al., 2010). In children, balance is inextricably linked to the mastering of basic motor skills (Fisher et al., 2005). Shah, Rao, Malawade, and Khatri (2013) reported that children with hearing impairments have balance and motor deficits that are primarily due to concomitant damage to the vestibular structures. In most hearing-impaired children, fundamental motor skills, such as the maintenance of head, sitting, and bipedal positions, develop much more slowly than in children with normal hearing (Rajendran and Finita, 2010). To master these skills, a properly developed body schema that is based on perception and experience is essential. Sensations from the skin, proprioceptive information from the muscles and joints, and motion- and gravity-related information from the vestibular system are organized, integrated, and ultimately applied during daily activities. Due to the well-organized perceptions of the body, an individual can feel the actions of any given part of the body, how those parts move, and where those parts are in space. However, when the supply of information from one of the sensory systems is limited, for example, due to the loss of hearing, the feeling of one’s body within space may be affected, and result in a reduction of the maturity level of posture control (An, Yi, Jeon, & Park, 2009). Such reduced maturity levels can be particularly dangerous when the flow of information from another system, such as the visual system, is obstructed (e.g., when walking in the dark or riding a bicycle at dusk). Simultaneously, the poor postural control abilities of the deaf during childhood do not necessarily entail difficulties in the performance of everyday activities during adulthood (Kaga, 1999). Postural reactions may be well-developed in adolescence despite irregularities in the impulses received from the vestibular system due to the compensatory responses of the other systems. Therefore, it is important to examine the severities of the disorders of balance reactions that occur in hearing-impaired children and how such severities depend on the flow of information from other systems. Such evaluations may facilitate the decision to introduce measures to stimulate the relevant sensory systems as early as possible. 2. Objectives The aim of this study was to evaluate the severities of the disorders of balance reactions that occur in a group of children with profound hearing loss relative to children with normal hearing. 3. Methods 3.1. Participants The study examined a total of 228 children, including 65 subjects who were deaf (DCH) aged between 8 and 17, and a control group of 163 subjects without any hearing deficits aged between 8 and 16 (CON) (Table 1). This study was conducted in four schools in Rzeszo´w and two schools for hearing-impaired children in the Subcarpathian region of Poland. The 25 (38.46%) of participants with hearing loss been hearing impaired since birth, and 40 (61.54%) had hearing disorders acquired later. The general criterion for inclusion in this study was the lack of neurological and orthopedic disorders. Additional inclusion criteria were, for the study group, a degree of deafness 90 dB and, for the control group, a complete lack of hearing deficits. Exclusion criteria included: an intellectual disability and comorbid illnesses. This study was approved by the local Bioethical Committee and performed after obtaining written consent from the children’s parents. 3.2. Procedure First, the parents of the children completed a questionnaire. The following information was acquired via questionnaire filled by parents: date of birth, illness, and degree of deafness. In the second part of the study, stabilometric measurements Table 1 Characteristics of the subjects.
Number of subjects Sex Male Female Age [mean SD]
Hearing-impaired children
Children with normal hearing
65
163
46 19 13.4 (2.4)
79 84 11.9 (2.2)
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were performed with a force distribution platform that was produced by Zebris WinPDMS. Sign language was used to communicate with the deaf children. Static standing position with eyes open and then closed was tested (Giagazoglou et al., 2013; Haidan et al., 2008; Harringe et al., 2008). The subjects were instructed to maintain an upright position with their arms at their sides and their eyes fixed on a black point located 1.5 meters away while standing barefoot on the platform. The position of the black point was adjusted to for the heights and eye levels of the subjects. As previous studies (Ruhe, Fejer, & Walker, 2010; Scoppa, Capra, Gallamini, & Shiffer, 2013) have not provided clear guidelines concerning foot positions, the subjects were instructed to place their feet along the designated lines on the platform while maintaining a relaxed, natural position in which their feet were no more than hip-width apart. Simultaneously, the subjects were asked to refrain from shaking their heads, moving their arms, or turning during the test. To minimize any external effects, the tests were performed in a quiet room in which only the person being examined was present. The tests lasted 30 s, of which 20 s were recorded (Di Nardi, 2010). The first 10 s were spent preparing for the examination to eliminate uncontrolled center of pressure (COP) movements (Derlich, Kre˛cisz, & Kuczyn´ski, 2011). According to a typical procedure that has been utilized in similar studies, each participant performed 3 trials (Ruhe et al., 2010) for each of two tests. 3.3. Data analysis Static balance testing was performed on a Zebris WinPDMS platform, which measures the pressure distribution of static forces. The WinPDMS system analyses the statical pressure distribution in real-time. The platform has dimensions 600 mm 380 mm 20.1 mm (B H T) and 1536 pressure sensors with pressure measurement ranges 1–120 N/cm2 and a resolution of 1 sensor/cm2 sensor area 320 mm 480 mm. The sensors respond to load changes of the lower limbs. The testing was performed while data were recorded at the recommended sampling frequency of 20 Hz (Słomka, Juras, Sobota, & Bacik, 2013). Following registration, the system automatically performed basic analyses of the captured signals for stabilometric assessment. Multiple COP deflection during the test are marked with lines that create a different size elipse. The ellipse includes 95% of the COP. Characteristics of the circle are displayed in a chart. Balance was evaluated based on the average results obtained across the three trials (Ruhe et al., 2010) based on the following parameters: left leg COP in the front (LLF – mm), left leg COP in the back (LLB – mm), whole left leg COP (LLW – mm), right leg COP in the front (RLF – mm), right leg COP in the back (RLB – mm), whole right leg COP (RLW – mm), the width of the ellipse delineated by the COP (WE – mm), the height of the ellipse delineated by the COP (HE – mm), the angle of the ellipse delineated by the COP indicates the orientation of the direction of the longitudinal axis of the ellipse compared to the longitudinal (x-) axis of the platform in degree and the orientation direction (left or right) (AE – deg), the area of the ellipse (ARE – mm2), the total path length of the COP (TPL – mm), the horizontal sway of the COP (HS – mm), and the vertical sway of the COP (VS – mm). 3.4. Analysis Independent assessments were performed for each group. The normalities of the posturographic parameter distributions were examined with the Kolmogorov–Smirnov test. The analysis revealed that, of the 52 total analyses, the data from 24 were not normally distributed; thus, we decided to perform all analyses using nonparametric methods to harmonize the statistical results. In addition to the mean values, the medians were used for statistical description (because the median is a more reliable indicator of the characteristics of a non-normally distributed parameter). Comparisons between groups were performed using the Mann–Whitney U test for independent samples. 4. Results The results revealed statistically significant differences between the groups in terms of one parameter (i.e., total path length of the COP – TPL) that was recorded during the open-eye test (Table 2) and many parameters that were recorded during the closed-eye test (Table 3). The results from the hearing-impaired children during the eye-closed test were lower, (i.e., better) than those children from control group during the eye-open test, particularly in terms of the area (ARE), width (WE) and height (HE) of the ellipse that was delineated by the COP. The results from the children with normal hearing were similar across the two tests. Our analyses revealed that the hearing-impaired children exhibited lower (i.e., better) static balance parameters than did their normal hearing peers and that these differences were particularly evident in the closedeye test. Mann–Whitney U tests revealed significant differences in the total path lengths of the COPs (TPLs) in both tests (i.e., the open- and closed-eye tests). Additionally, in the open-eye test, the hearing-impaired children exhibited significantly lower values than did the children with normal hearing in the parameters of the area (ARE), width (WE) and height (HE) of the ellipse delineated by the COP and in the parameters of horizontal and vertical sway of the COP (HS and VS, respectively) (Table 3). 5. Discussion Hearing loss affects between 1 to 6 of every 1000 children worldwide, and among the affected children, 10% have profound hearing deficits (Rajendran & Roy, 2011). Due to the close relationship between the auditory and vestibular
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Table 2 Comparison of posturographic parameters recorded for the hearing-impaired and children with normal hearing children in the open-eye test. Parameter
1 2 3 4 5 6 7 8 9 10 11 12 13
LLF [mm] LLB [mm] LLW [mm] RLF [mm] RLB [mm] RLW [mm] WE [mm] HE [mm] AE [deg] ARE [mm2] TPL [mm] HS [mm] VS [mm]
Hearing-impaired children
Children with normal hearing
Mean
Median
Mean
Median
34.2 67.0 49.6 37.3 62.8 48.8 6.7 13.7 26.0 99.4 527.9* 3.6 4.9
33.1 69.5 49.3 35.7 63.6 50.4 5.5 10.0 16.8 43.3 496.5 2.7 3.9
31.6 68.4 50.2 33.6 66.4 49.8 6.7 13.5 28.4 78.5 1083.6 3.5 4.9
30.4 69.6 50.2 32.4 67.6 49.8 6.2 12.0 21.9 59.7 1059.3 3.2 4.4
Mann–Whitney U test
Significance level
4798.50 4967.00 4883.50 4545.50 4524.50 5115.00 4569.00 4449.00 4958.50 4484.00 664.00 4650.50 4598.00
.267 .462 .357 .094 .086 .685 .105 .059 .451 .070 .000 .150 .120
Parameters: left leg COP in the front (LLF), left leg COP in the back (LLB), whole left leg COP (LLW), right leg COP in the front (RLF), right leg COP in the back (RLB), whole right leg COP (RLW), width of the ellipse delineated by the COP (WE), height of the ellipse delineated by the COP (HE), angle of the ellipse with respect to the horizontal level (AE), area of the ellipse (ARE), total path length of the COP (TPL), horizontal sway of the COP (HS), and vertical sway of the COP (VS). * Statistically significance difference between the hearing-impaired and children with normal hearing (P 0.001).
Table 3 Comparison of the posturographic parameters recorded from the hearing-impaired and children with normal hearing in the closed-eye test. Parameter
1 2 3 4 5 6 7 8 9 10 11 12 13
LLF [mm] LLB [mm] LLW [mm] RLF [mm] RLB [mm] RLW [mm] WE [mm] HE [mm] AE [deg] ARE [mm2] TPL [mm] HS [mm] VS [mm]
Hearing-impaired children
Children with normal hearing
Mean
Median
Mean
Median
33.2 67.3 49.8 36.4 63.6 49.9 6.0* 12.6* 27.8 80.0* 529.6* 3.13** 4.69*
30.5 69.8 49.5 31.7 68.3 50.3 4.7 10.2 18.4 40.0 499.2 2.60 3.80
31.8 68.2 49.6 33.6 66.4 50.4 7.5 14.8 21.0 107.6 1108.4 3.56 5.72
29.7 70.3 49.4 32.5 67.5 50.6 6.5 13.7 12.9 70.2 1061.6 3.00 5.20
Mann–Whitney U test
Significance level
4892.50 5003.00 5205.50 4803.00 4823.50 5162.50 3749.00 3557.00 4534.00 3580.00 482.00 4111.00 3422.50
.368 .512 .838 .271 .292 .764 .001 .000 .090 .000 .000 .008 .000
Parameters: see the legend for Table 2. * P 0.001 for the differences between the hearing-impaired and children with normal hearing. ** P 0.01 for the differences between the hearing-impaired and children with normal hearing.
systems, it can be assumed that deaf children are at risk for deficits in body balance (Cushing, Papsin, Rutka, James, & Gordon, 2008). Balance reactions are responses to integrated stimuli that are delivered by proprioceptive and exteroceptive sensations, telereceptors, and the vestibular system; therefore, disorders in the reception of these stimuli from any of these receptors or systems can result in impaired stability (Sousa, Franca Bartos, & de Sousa Neto, 2012). The tests that are used in studies that assess balance function include static tests (i.e., the fulcrum of the body is fixed) and dynamic tests (i.e., the fulcrum of the body changes). The most well-known tests comprise a traditional test that involves standing on one leg, Romberg’s test, the Berg Balance Scale, the Fullerton Advanced Balance (FAB) test, and the Scale and Tapping test (i.e., the Fleishman test). More accurate and reliable diagnostic methods for the analysis of the static balance of hearing-impaired children, like those used in the current study, involve computer graphic records of shifts in the center of gravity that are via stabilometric platforms (the so-called posturographic tests) (Kostiukow, Rostkowska, & Samborski, 2009). The current results suggest that the processing of sensory stimuli during postural reactions, particularly stimuli from propioception and to a lesser extent from the visual system, was significantly better in the hearing-impaired subjects than in the control group. These finding agree with the ‘‘sensory compensation’’ hypothesis, which states that the loss of one sensory modality induces compensations in the other intact sensory modalities (Lo´pez-Crespo, Daza, & Me`ndez-Lo´pez, 2012). Our results can be explained by the fact that visual orienting is not essential for the maintenance of postural
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stability during static, quiet standing (Westcott, Lowes, & Richardson, 1997). Postural reactions are also based on information from the proprioceptors and the vestibular system (i.e., somatosensory and vestibular inputs). Only the integration of information that is received from the so-called active sensory channels affects the final postural response (Szymczyk, Druz˙bicki, Dudek, Szczepanik, & Snela, 2012). The results of this study may explain the reports of other authors who have confirmed that the most important information for maintaining balance in the upright position, even when the support surface is distorted, is the information from the proprioreceptors (Shumway-Cook & Woollacott, 2006). In contrast, visual stimuli are used in more difficult balance situations (Sundermier, Woollacott, Jensen, & Moore, 1996), and, in such situations, the vestibular system has a lesser role than does the sensory information (Dietz, Schubert, Discher, & Trippel, 1994). Findings similar to ours were reported by Wierzbicka-Damska, Samołyk, Jethon, Wiercin´ska, and Murawska-Ciałowicz (2005) who examined 29 hearing-impaired children and 38 hearing children aged 10–16 years on a stabilometric platform and observed superior better stabilometric values among the children with impaired hearing. The same conclusion has been reached by the authors of other studies (Kaga, 1999; An et al., 2009) who have suggested that children with hearing loss can manifest relatively normal postural reactions due to the adaptations afforded by sensory compensation. Moreover, the results of clinical balance tests that were conducted by De Kegel et al. (2011) revealed excellent overall test–retest reliabilities (ICCs above 0.80) in children with normal hearing and hearing-impaired children (ICCs above 0.90). Similar to the results of our study, in this aforementioned study, the area of the ellipse delineated by the COP was nearly two-fold lower in the hearing-impaired children than in the typically developing children. It means that hearing impaired children had two times better results of this stabilometric test, their COP inclination was smaller. However, in another study (De Kegel, Maes, Baetens, Dhooge, & Van Waelvelde, 2012), these same authors concluded that hearing-impaired children are at risk for balance deficits. Some authors have indicated that static balance reactions in children with profound hearing loss can be weakened. Similar studies were conducted by Jernice et al. (2011). Authors have suggested that the parameters of children with hearing-impairments during static tests of standing on one leg with the open and closed eyes are lower than those of health controls. The higher mean path length (MPL) and root mean square (RMS) value were recorded in the anterior–posterior plane (AP) and the medial–lateral plane (ML) confirm the weaker balance capabilities of hearing-impaired children. Nevertheless, the analyses of these research materials revealed that these results were not confirmed in a larger sample of subjects (Tan, Nonis, & Chow, 2011). Similar conclusions have been presented by researchers from Iran who found that, in a group of 30 children with profound hearing loss, 16.7–100% of the children were characterized by the incorrect execution of a balance task over seven trials (Jafari, Malayeri, Rezazadeh, Haji, & Heydari, 2011). The majority of reports of research on the dynamic balance of children with hearing impairments indicate reduced functionality (Rahman, 2005). The study conducted by Wong, Leung, Poon, Leung, & Lau (2013) showed that children with severe-to-profound-grade hearing impairments exhibited balance deficits as assessed with the Bruininkse–Oseretsky test of Motor Proficiency (BOT2), the Pediatric Functional Reach Test (FRT), the Pediatric Version of the Clinical Test for Sensory Interaction of Balance (P-CTSIB) and the Test of Postrotary Nystagmus (PRN). The present results and the results of other authors do not unequivocally prove that children with hearing impairment have significantly worse postural stabilities than do their hearing peers. Further research in this area is necessary to obtain definite conclusions.
6. Limitations We acknowledge some limitations in this study. One of the most relevant limitations is the lack of a standard, reliable, validated outcome measure for the assessment of static balance in children. The balance parameters and their modified versions that were used in this work have been widely used to assess people with normal hearing and patients with different illnesses. Other limitations of our study include the difference in the numbers of hearing impaired and children with normal hearing and the fact that we used a single observation of the children’s static balance. Similar differences in the numbers of typically developing and hearing impaired children were present in other studies; for example, in the study conducted by De Kegel et al. (2011), the ratio of typically developing to hearing impaired children was 2.1–1.0. The main reason for this problem is probably related to the presence of numerous significant inter-population differences. We plan conduct further assessments in this area utilizing equal numbers of hearing-impaired and children with normal hearing and repeated measurements. Additionally, it will be important to perform measurements of dynamic equilibrium in groups of hearing-impaired children to determine the correlations between the recorded parameters and the degree of hearing loss. The lack of a comparison between the static and dynamic measures of postural stability in this current study precludes the identification of (1) differential responses between the hearing-impaired and children with normal hearing for the maintenance of postural stability and (2) the different stresses on the systems that are necessary for the maintenance of postural stability under different dynamic conditions. Some authors have concluded that dynamic measures of postural stability are more difficult to obtain but are also more informative. Lastly, in the present study, we were unable to examine whether gender differences may have influenced postural stability.
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7. Conclusions The results of the present study revealed that the hearing-impaired children exhibited superior static balance parameter values than did their children with normal hearing peers and that these differences were particularly evident in the closedeye test. Our results suggest that the hearing-impaired children exhibited significantly better processing of sensory stimuli in postural reactions, particularly proprioception stimuli and to a lesser extent visual stimuli, than did their peers in the control group. References An, M. H., Yi, C. H., Jeon, H. S., & Park, S. Y. (2009). Age-related changes of single-limb standing balance in children with and without deafness. International Journal of Pediatric Otorhinolaryngology, 73, 1539–1544. Chilosi, A. M., Comparini, A., Scusa, M. F., Berrettini, S., Forli, F., Battini, R., et al. (2010). Neurodevelopmental disorders in children with severe to profound sensorineural hearing loss: A clinical study. 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