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Age-related changes of single-limb standing balance in children with and without deafness
International Journal of Pediatric Otorhinolaryngology 73 (2009) 1539–1544
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Age-related changes of single-limb standing balance in children with and without deafness Mi-hee An a, Chung-hwi Yi b,c,*, Hye-seon Jeon b,c, So-yeon Park d a
Department of Rehabilitation Therapy, The Graduate School, Yonsei University, 234, Maeji-ri, Heungup-myun, Wonju, Kangwon-do 220-710, Republic of Korea Department of Physical Therapy, College of Health Science, Yonsei University, 234, Maeji-ri, Heungup-myun, Wonju, Kangwon-do 220-710, Republic of Korea c Department of Ergonomic Therapy, The Graduate School of Health and Environment, Yonsei University, 234, Maeji-ri, Heungup-myun, Wonju, Kangwon-do 220-710, Republic of Korea d Department of Physical Therapy, College of Alternative Medicine, Jeonju University, Hyoja-dong 3-ga, Wansan-gu, Jeonju-si, Jeonbuk 560-759, Republic of Korea b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 January 2009 Received in revised form 25 May 2009 Accepted 25 July 2009 Available online 31 August 2009
Objective: The purposes of the present study were to elucidate the age-related changes in single-limb standing balance and sensory compensation for maintaining single-limb standing in profoundly deaf (PD) children, and to compare them with age-matched normal-hearing (NH) children. Methods: This study involved 57 PD children, aged 4–14 years and 57 age-matched NH children. Each group was subdivided into the following age groups: 4–6 years, 7–9 years, and 12–14 years. Postural stability was assessed using a single-limb standing test under four different sensory conditions: standing on a firm surface with eyes open (condition 1), standing on a firm surface with eyes closed and covered (condition 2), standing on a foam surface with eyes open (condition 3), and standing on a foam surface with eyes closed and covered (condition 4). Results: The age-related changes in single-limb standing balance of the PD children were notably affected by sensory conditions, in contrast with those of the NH children, which were not influenced by sensory conditions. In conditions 1 and 3, where visual information was enabled, the mean time of maintaining single-limb standing for the PD children significantly increased with age, and even reached levels similar to those of the NH children. However, in condition 2, where visual input was removed, the deficit of single-limb standing balance in the PD children persisted. Condition 4 revealed no significant age-related changes in the PD children. Conclusion: These results suggest that the postural stability of PD children improves as a result of adaptive sensory compensation, both visual and somatosensory. In addition, it appears that postural control is more highly dependent upon visual input than on somatosensory input. ß 2009 Elsevier Ireland Ltd. All rights reserved.
Keywords: Children Deafness Sensory compensation Single-limb standing balance Somatosensory Vision
1. Introduction The development of postural stability involves dynamic interactions between multisensory networks, including the visual, somatosensory, and vestibular systems. Each sensory system provides the central nervous system (CNS) with specific information about the position and motion of the body [1]. According to developmental studies, the visual system plays a predominant role in the development of postural stability in young children, while somatosensory and vestibular inputs appear to dominate postural control later in life [2,3]. Researchers have found that postural control is essentially adult-like by 7–10 years of age, which means
* Corresponding author at: Department of Physical Therapy, College of Health Science, Yonsei University, 234, Maeji-ri, Heungup-myun, Wonju, Kangwon-do 220-710, Republic of Korea. Tel.: +82 33 760 2429; fax: +82 33 760 2496. E-mail address: [email protected] (C.-h. Yi). 0165-5876/$ – see front matter ß 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2009.07.020
that children over the age of 7 years easily maintain postural stability during both quiet and perturbed stances [4]. Abnormal or delayed postural development is a common sensorimotor impairment in profoundly deaf (PD) children and is often associated with vestibular dysfunction [5,6]. Previous studies have found that 49–95% of children with hearing loss suffered from vestibular dysfunction, with the incidence increasing with the degree of hearing loss [7]. The cochlear and vestibular systems are anatomically and functionally connected, and so damage to either the cochlear or vestibular systems, or both, can lead to vestibular disorder and associated balance dysfunction [8]. Previous studies have also demonstrated that children with hearing loss show a significant increase in center-of-pressure deviation and body-sway velocity measures made during a static standing balance test, and in the balance performance measure of the subsection item of the Bruininks-Oseretsky Test of Motor Proficiency (BOTMP), when compared to normal-hearing (NH) children [8–11].
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It remains to be established unequivocally whether or not postural stability in PD children develops adequately with age. Previous developmental studies have proposed that PD children can exhibit gradually or consistently retarded development of postural stability [8–11]. Rine et al. [8] repeatedly examined the balance and gross motor development of children with hearing loss and found that most of the children showed a significantly poor performance in both the balance and gross motor tests. These findings suggest that postural development in PD children is delayed progressively. In addition, other studies have shown that delayed postural development in children with hearing impairment persists but does not worsen [9–11]. Carlson [10] assessed PD children aged 5–10 years using the Brace Motor Ability Test, and found that the motor development of these children adaptively improved up to 7 years of age and then plateaued. In addition, Siegel et al. [11] examined children with hearing loss in three different age groups (4.5–6.5 years, 8–10 years, and 12.5–14.5 years) using the balance subtest of the BOTMP in order to determine age-related changes in balance ability. The results of the comparison with the normative data showed that the balance ability of children with hearing loss improves until they reach approximately 10 years of age, after which any existing deficits persist. According to a study by Brunt and Broadhead [9], the balance ability of children with hearing loss improves with age but remains lower than that of NH children at the age of 7–14 years. On the other hand, studies of postural stability in patients with vestibular dysfunction have shown that the degree of postural sway during quiet stance is normal in conditions under which either visual or somatosensory input is enabled. In contrast, they have a hard time maintaining postural stability when both visual and somatosensory inputs are inadequate [12,13]. Empirical research suggests that older children with hearing impairment have relatively functional postural stability as a result of the contribution of adaptive sensory compensation [5,12,14]. According to a study by Kaga [5], vestibular loss in children with hearing loss is nearly completely compensated for by the contribution of the visual and somatosensory systems, and by the plasticity of the CNS, by 10 years of age. Suarez et al. [6] examined postural control in children with hearing impairment at 8–11 years of age under two different sensory conditions: standing on a firm surface with eyes open (condition 1) and standing on a foam surface with eyes closed (condition 2). The children with hearing impairment found it difficult controlling their upright posture in condition 2, where visual information was removed and somatosensory information was modified. Recent studies have focused on age-related changes in the postural development of children with hearing impairment, but their findings remain equivocal. In addition, few previous studies have examined sensory compensation of children with hearing impairment and compared this in age-matched NH children. The study presented here was thus designed to elucidate the agerelated changes in single-limb standing balance and sensory compensation for maintaining postural stability in altered sensory conditions in PD children. The results are compared with those of age-matched NH children. 2. Method 2.1. Subjects The study involved 57 PD children aged 4–14 years of age and 57 age-matched NH children (Table 1). The children were recruited from two local elementary schools, a middle school, and three schools for the deaf. Each group was subdivided according to age: group 1, 4–6 years; group 2, 7–9 years; and group 3, 12–14 years. Inclusion criteria for the PD group included a hearing loss greater
Table 1 Characteristics of the subjects (n = 114). Hearing ability
Age group
Children with deafness (n1 = 57)
4–6 years 7–9 years 12–14 years 4–6 years 7–9 years 12–14 years
Children with normal hearing (n2 = 57)
Gender Male
Female
7 12 14 8 12 12
11 7 6 10 7 8
than 70 dB; we did not determine the etiology of the hearing loss. Exclusion criteria for all subjects included any neuromuscular or musculoskeletal condition, uncorrected visual disability, and learning disability as identified from school records. The subjects and their parents were informed about the purpose, procedures, and applications of this study, and parental agreement for their children to participate was obtained. 2.2. Experimental equipment The equipment used included a silent stopwatch that can measure centesimal units, eye bandages, and 5-cm-thick foam sponges. 2.2.1. Single-limb standing test (SLS) The single-limb standing test is a commonly used clinical tool for the measurement of standing balance. It assesses postural stability in a static standing position by measuring the time (in seconds) a subject can maintain the single-limb standing position. Atwater et al. [15] have shown that the single-limb standing test has good interrater reliability (r = 0.87–0.99) and fair-to-good test– retest reliability (r = 0.59–1.00) in both the eyes open and eyes closed conditions. 2.3. Procedure We administered a static standing balance test in a quiet classroom in the schools. Before testing, each child was required to kick a ball to define his or her dominant leg, which was used for the balance test. Static standing balance was assessed with the singlelimb standing test under four different sensory conditions: standing on a firm surface with eyes open (condition 1), standing on a firm surface with eyes closed and covered (condition 2), standing on a foam surface with eyes open (condition 3), and standing on a foam surface with eyes closed and covered (condition 4). The test was performed twice for each condition and the better performance was recorded. The children were allowed to rest for 1 min between tests to prevent muscle fatigue. The four conditions were administered in a random order by drawing lots. All directions were explained to each subject via total communication, which involves speech, sign language, body language, and demonstration. The subjects were instructed to stand on one leg for as long as possible but for a maximum of 60 s for each trial. They were barefoot and positioned 2 m from a wall upon which a visual target had been placed at their eye level. When standing with eyes open during the test (conditions 1 and 3), the subjects were instructed to look at the target. When standing with eyes closed (conditions 2 and 4), an eye bandage was used to cover the subject’s eyes in order to prevent them from furtively opening them. The subjects were instructed to place their hands on their hips, raise their nondominant leg behind them with their knee bent at 908 and shin parallel to the floor, and to look at the target. For all conditions, timing was started as soon as the angle of knee became 908 with the shin parallel to the floor. Timing was stopped when the
M.-h. An et al. / International Journal of Pediatric Otorhinolaryngology 73 (2009) 1539–1544
subjects touched the raised foot to the floor, took their hands off of their hips, or shifted the supporting foot from the starting position. Timing was also stopped if the subject continued to hook the raised leg behind the support leg after two warnings, or failed to keep the raised leg lifted to at least the mid-range of knee flexion. 2.4. Statistical analysis The primary analysis was repeated-measures analysis of variance (ANOVA), with age as the between-subjects factor and condition as the within-subject factor. Eight separate one-way ANOVAs were then used to determine the age-related changes of single-limb standing balance in PD and NH children in altered sensory conditions. Where the one-way ANOVA showed a significant difference, Bonferroni’s adjustment was used to identify where specific differences occurred. Two-way ANOVAs (age hearing ability) by condition were used to determine if there were differences in single-limb standing balance depending on the hearing ability. Independent t-tests were also used to verify if there were differences in the mean single-limb standing time between the PD and NH children in each age group. The SPSS statistical package was used to analyze differences in single-limb standing balance in PD and NH. Hypothesis testing was carried out with a = 0.05. 3. Results 3.1. General single-limb standing balance Table 2 lists the mean time for maintaining postural stability in the single-limb standing balance test. Single-limb standing balance in both the PD and NH group was significantly different depending on age (Tables 3, 5 and 7). In general, the PD group demonstrated significantly lower single-limb standing balance than the NH group (Fig. 1) (Table 3).
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3.2. Age-related changes in single-limb standing balance Repeated-measures ANOVAs showed significant main effects for age and condition in both the PD and NH groups. There was an interaction, however, between age and condition in the PD group, but not in the NH group (Fig. 2) (Tables 4–7), which indicates that the age-related changes in single-limb standing balance in the PD group were affected by the sensory conditions, in contrast with those in the NH group, which were not affected by the sensory conditions (Fig. 3). The independent t-test, which was used to compare the mean single-limb standing time of the PD children with the age-matched NH children, indicated a significant difference in single-limb standing balance within each age group, depending on the condition and age. In age group 1, there were significant differences between the PD and NH children under all conditions. These differences diminished with age, however, except for condition 2, where the difference between both groups persisted regardless of age (Fig. 1). 3.3. Single-limb standing balance under specific sensory condition The single-limb standing balance of the PD children was significantly lower than that of the NH children. In specific sensory conditions, however, where visual information was enabled, the single-limb standing balance of the PD group improved with age and reached a level similar to that seen in the NH group. Fig. 3 shows the age-related changes in single-limb standing balance under specific sensory conditions. In condition 1, the mean time for the PD group significantly increased with age, but an increase in the mean time for the NH group was only observed in a comparison between age group 3 (12–14 years) and age group 1 (4–6 years). In condition 2, both the PD and NH groups showed a significant difference between age groups 1 and 3 only. In condition 3, significant increases were found between age groups 1 and 2, and age groups 1 and 3 among the PD
Table 2 Time for maintaining one-leg standing balance by age group and sensory condition (unit: seconds). Age group (years)
Condition Condition Condition Condition
1 2 3 4
PD group (n1 = 57)
NH group (n2 = 57)
4–6 (n = 18)
7–9 (n = 19)
12–14 (n = 20)
4–6 (n = 18)
7–9 (n = 19)
12–14 (n = 20)
4.33 4.66a 1.89 1.38 2.46 1.91 1.23 0.59
21.61 7.28 4.26 4.14 17.33 9.03 3.07 2.25
37.16 17.96 4.89 3.82 28.61 18.12 4.32 7.12
37.55 21.11 9.19 7.29 33.62 21.60 4.96 4.67
42.99 9.63 10.06 9.63 34.23 20.36 5.43 4.13
53.35 12.18 18.98 16.38 45.93 18.81 9.98 13.08
PD: profoundly deaf; NH: normal hearing. Condition 1: eyes open, firm surface; condition 2: eyes closed, firm surface Condition 3: eyes open, foam surface; condition 4: eyes closed, foam surface. a Mean SD. Table 3 Summary for the two-way ANOVA by condition.
Condition 1
Condition 2
Condition 3
Condition 4
Age Hearing ability Age hearing ability Age Hearing ability Age hearing ability Age Hearing ability Age hearing ability Age Hearing ability Age hearing ability
Type III sum of squares
df
Mean square
F
p
11253.022 15843.688 1426.976 852.650 2336.673 382.464 7150.557 13512.347 1215.820 335.303 436.461 53.719
2 1 2 2 1 2 2 1 2 2 1 2
5625.511 15843.688 713.488 426.325 2336.673 191.731 3575.278 13512.347 607.910 167.651 436.461 26.190
20.583 57.960 2.610 5.556 30.453 2.492 11.053 41.773 1.879 3.630 9.449 .581
.000** .000** .078 .005** .000** .087 .000** .000** .158 .030* .003** .561
Age and hearing ability were the main factors affecting single-limb standing balance under four different conditions in children. * p < 0.05. ** p < 0.01.
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Fig. 1. Comparison using the independent t-test of the mean time for maintaining single-limb standing between PD and NH children (*p < 0.05, **p < 0.01). The deficit in the PD children’s single-limb standing balance dwindled with age in conditions 1 and 3, in which visual information was enabled. In condition 2, however, in which visual input was removed, the deficit in the PD children’s single-limb standing balance persisted. Condition 1: eyes open, firm surface; condition 2: eyes closed, firm surface; condition 3: eyes open, foam surface; condition 4: eyes closed, foam surface. Age group 1: 4–6 years; age group 2: 7–9 years; age group 3: 12–14 years.
children; no significant differences were found in the NH children. In condition 4, both the PD and NH groups showed no statistically significant differences between any age group. 4. Discussion Vision is important during quiet stance, but it is not absolutely necessary to maintain postural stability because not only visual but also somatosensory and vestibular inputs all influence quiet stance postural control. However, there were significant agerelated changes among the PD children in both condition 1, where visual information was enabled, and condition 2, where visual input was obscured, although the improvement with age was much greater in condition 1 than in condition 2. In contrast, NH children showed a similar result in the comparison of both conditions. This indicates that the single-limb standing balance of children who are PD improves as a result of the provision of visual information rather than somatosensory inputs, and this dependence become essential with age. In addition, our finding that the improvement of single-limb standing balance seen under condition 1 was continuous until age group 3 (12–14 years) is
inconsistent with the finding of Kaga’s study [5] that vestibular dysfunction in children with hearing impairment is compensated for by visual and somatosensory inputs by 10 years of age. The PD children showed obvious age-related improvements in single-limb standing balance under condition 3, where visual information was enabled and the supporting surface was perturbed. This differs from the observations in NH children, who demonstrated no significant differences with age, indicating that PD children compensate for their postural instability using somatosensory and visual information. Somatosensory information is the most important for maintaining standing balance on a perturbed supporting surface [4], but a difficult balance task is associated with a higher reliance on visual cues [16]. Moreover, vestibular responses to support-surface perturbation appear to be much smaller than those of somatosensory input [17]. Thus, under condition 3, the PD children might have compensated for their postural instability by using visual and somatosensory information. When children were examined under condition 4, no agerelated changes in single-limb standing balance were seen in either the PD or NH groups. Since the information provided by the
Fig. 2. Comparisons between sensory conditions for maintaining single-limb standing in each age group. This figure shows an interaction between age and condition in the PD group but not in the NH group. Age group 1: 4–6 years; age group 2: 7–9 years; age group 3: 12–14 years. Condition 1: eyes open, firm surface; condition 2: eyes closed, firm surface; condition 3: eyes open, foam surface; condition 4: eyes closed, foam surface.
M.-h. An et al. / International Journal of Pediatric Otorhinolaryngology 73 (2009) 1539–1544 Table 4 Multivariate tests performed on the data of mean time of maintaining single-limb standing in PD children. Effect
Value
F
Hypothesis df
Error df
p
Condition Condition age
0.357 0.541
31.277 6.235
3.000 6.000
52.000 104.000
0.000 0.000
The PD children’s single-limb standing balance was affected by condition and age, and there was an interaction between the two.
Table 5 Between-subject tests of the effect on the mean time for maintaining single-limb standing in PD children.
Age
Type III sum of squares
df
Mean square
F
p
2509.874
2
1254.937
21.746
0.000
Table 6 Multivariate tests performed on the data of mean time of maintaining single-limb standing in NH children. Effect
Value
F
Hypothesis df
Error df
p
Condition Condition age
0.173 0.907
83.100 0.872
3.000 6.000
52.000 104.000
0.000 0.518
The NH children’s single-limb standing balance was affected by condition and age, and there was no interaction between the two.
Table 7 Between-subject tests of the effect on the mean time for maintaining single-limb standing in NH children.
Age
Type III sum of squares
df
Mean square
F
p
1273.932
2
636.966
4.831
0.000
vestibular system, which is inertial and gravitational, is not affected by the environmental context, vestibular information is important for resolving the intersensory conflict [13,18]. When children maintain their single-limb standing balance under eyes closed, compliant-foot-support conditions, such as condition 4, the
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vestibular inputs are essential in providing an absolute reference for postural control. However, vestibular function develops more slowly than do visual and somatosensory functions [13,19]. Hirabayashi and Iwasaki [18] studied the development of sensory organization on postural control under various sensory conditions using computerized dynamic posturography. They measured the subjects’ sway, calculated from the maximum displacement of the center of gravity, while they (112 children aged 3–15 years and 26 adults aged 20–60 years) stood under 6 different sensory conditions. Their results show that vestibular function had not reached the adult level even at the age of 14–15 years. Since all children who participated in the present study were under 15 years of age, it is likely that their vestibular function had thus not yet matured. This is the most likely reason why no age-related changes in single-limb standing balance were observed in either the PD or NH children. Our results can be explained by the concept of sensory weighting, which asserts that people maintain their postural stability based on the relative accuracy of sensory input reporting the body’s position and movement in space [13,20]. When a sense provides inaccurate information, the weight given to that sense is reduced, while the weight of other senses that continue to provide more accurate information is increased [4]. Based on the concept of sensory weighting, PD children who might also have vestibular dysfunction might be more reliant on visual and somatosensory information, which is putatively more reliable than vestibular information. In the present study, when visual information was enabled but somatosensory input was inaccurate, as in condition 3, single-limb standing balance in the PD children improved with age and even reached at levels similar to those of the NH children. However, when visual information was enabled and somatosensory input was accurate, as in condition 1, single-limb standing balance in PD children increased with age but remained lower than that of the NH children. Furthermore, when visual information was unable but somatosensory input was accurate, as in condition 2, single-limb standing balance improved just a little. These findings indicate that although children with hearing impairment do compensate for their vestibular dysfunction with visual and somatosensory inputs, the dependence on visual input is greater than on somatosensory input.
Fig. 3. Between age group comparisons using eight separate one-way ANOVAs with Bonferroni’s adjustment. Mean time in each age group for maintaining single-limb standing under four sensory conditions (*p < 0.05, **p < 0.01). The older PD children’s single-limb standing balance was significantly better than that of the younger PD children under certain sensory conditions where visual information was enabled. Age group 1: 4–6 years; age group 2: 7–9 years; age group 3: 12–14 years. Condition 1: eyes open, firm surface; condition 2: eyes closed, firm surface; condition 3: eyes open, foam surface; condition 4: eyes closed, foam surface.
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In summary, the single-limb standing balance of older PD children improves by adaptive sensory compensation, in contrast to younger PD children, who show significant deficits in single-limb standing balance. However, the dependence upon visual input for maintaining postural stability is higher than on somatosensory input. If PD children continuously rely on vision for postural stability, they might have a hard time maintaining postural stability under conditions in which visual input is insufficient or has been removed. Parents and teachers should therefore be aware of possibly dangerous situations for such children, such as walking in the dark, and should work to prevent them from encountering this type of situation unattended. In addition, it might be useful for deaf children to train with the intention of developing their somatosensory functions. This developmental study was completed using the single-limb standing balance test, which provides a quantitative measure of postural stability. Although this clinical tool is reliable, using other accurate assessment equipment together might provide even more reliable and accurate data. In addition, we were unable to assess the true age-related changes of single-limb standing balance under condition 4 due to the limited age range of 4–14 years used in this study. Further research should examine a wider range of ages with greater numbers of children to more completely define the agerelated changes of postural control in PD children. 5. Conclusion The objective of this study was to determine any age-related changes in single-limb standing balance and sensory compensation in PD and NH children aged 4–14 years under normal and altered sensory conditions. The results of the single-limb standing balance testing demonstrated that postural stability in PD children improves with age under the specific sensory conditions used in our testing. The method of improvement was adaptive sensory compensation, which includes both visual and somatosensory inputs. However, since visual dependency was much higher than somatosensory dependency in the PD children, it is suggested that PD children should enhance their somatosensory functions in order to better maintain their postural stability.
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Age-related changes of single-limb standing balance in children with and without deafness Mi-hee An a, Chung-hwi Yi b,c,*, Hye-seon Jeon b,c, So-yeon Park d a
Department of Rehabilitation Therapy, The Graduate School, Yonsei University, 234, Maeji-ri, Heungup-myun, Wonju, Kangwon-do 220-710, Republic of Korea Department of Physical Therapy, College of Health Science, Yonsei University, 234, Maeji-ri, Heungup-myun, Wonju, Kangwon-do 220-710, Republic of Korea c Department of Ergonomic Therapy, The Graduate School of Health and Environment, Yonsei University, 234, Maeji-ri, Heungup-myun, Wonju, Kangwon-do 220-710, Republic of Korea d Department of Physical Therapy, College of Alternative Medicine, Jeonju University, Hyoja-dong 3-ga, Wansan-gu, Jeonju-si, Jeonbuk 560-759, Republic of Korea b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 January 2009 Received in revised form 25 May 2009 Accepted 25 July 2009 Available online 31 August 2009
Objective: The purposes of the present study were to elucidate the age-related changes in single-limb standing balance and sensory compensation for maintaining single-limb standing in profoundly deaf (PD) children, and to compare them with age-matched normal-hearing (NH) children. Methods: This study involved 57 PD children, aged 4–14 years and 57 age-matched NH children. Each group was subdivided into the following age groups: 4–6 years, 7–9 years, and 12–14 years. Postural stability was assessed using a single-limb standing test under four different sensory conditions: standing on a firm surface with eyes open (condition 1), standing on a firm surface with eyes closed and covered (condition 2), standing on a foam surface with eyes open (condition 3), and standing on a foam surface with eyes closed and covered (condition 4). Results: The age-related changes in single-limb standing balance of the PD children were notably affected by sensory conditions, in contrast with those of the NH children, which were not influenced by sensory conditions. In conditions 1 and 3, where visual information was enabled, the mean time of maintaining single-limb standing for the PD children significantly increased with age, and even reached levels similar to those of the NH children. However, in condition 2, where visual input was removed, the deficit of single-limb standing balance in the PD children persisted. Condition 4 revealed no significant age-related changes in the PD children. Conclusion: These results suggest that the postural stability of PD children improves as a result of adaptive sensory compensation, both visual and somatosensory. In addition, it appears that postural control is more highly dependent upon visual input than on somatosensory input. ß 2009 Elsevier Ireland Ltd. All rights reserved.
Keywords: Children Deafness Sensory compensation Single-limb standing balance Somatosensory Vision
1. Introduction The development of postural stability involves dynamic interactions between multisensory networks, including the visual, somatosensory, and vestibular systems. Each sensory system provides the central nervous system (CNS) with specific information about the position and motion of the body [1]. According to developmental studies, the visual system plays a predominant role in the development of postural stability in young children, while somatosensory and vestibular inputs appear to dominate postural control later in life [2,3]. Researchers have found that postural control is essentially adult-like by 7–10 years of age, which means
* Corresponding author at: Department of Physical Therapy, College of Health Science, Yonsei University, 234, Maeji-ri, Heungup-myun, Wonju, Kangwon-do 220-710, Republic of Korea. Tel.: +82 33 760 2429; fax: +82 33 760 2496. E-mail address: [email protected] (C.-h. Yi). 0165-5876/$ – see front matter ß 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2009.07.020
that children over the age of 7 years easily maintain postural stability during both quiet and perturbed stances [4]. Abnormal or delayed postural development is a common sensorimotor impairment in profoundly deaf (PD) children and is often associated with vestibular dysfunction [5,6]. Previous studies have found that 49–95% of children with hearing loss suffered from vestibular dysfunction, with the incidence increasing with the degree of hearing loss [7]. The cochlear and vestibular systems are anatomically and functionally connected, and so damage to either the cochlear or vestibular systems, or both, can lead to vestibular disorder and associated balance dysfunction [8]. Previous studies have also demonstrated that children with hearing loss show a significant increase in center-of-pressure deviation and body-sway velocity measures made during a static standing balance test, and in the balance performance measure of the subsection item of the Bruininks-Oseretsky Test of Motor Proficiency (BOTMP), when compared to normal-hearing (NH) children [8–11].
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It remains to be established unequivocally whether or not postural stability in PD children develops adequately with age. Previous developmental studies have proposed that PD children can exhibit gradually or consistently retarded development of postural stability [8–11]. Rine et al. [8] repeatedly examined the balance and gross motor development of children with hearing loss and found that most of the children showed a significantly poor performance in both the balance and gross motor tests. These findings suggest that postural development in PD children is delayed progressively. In addition, other studies have shown that delayed postural development in children with hearing impairment persists but does not worsen [9–11]. Carlson [10] assessed PD children aged 5–10 years using the Brace Motor Ability Test, and found that the motor development of these children adaptively improved up to 7 years of age and then plateaued. In addition, Siegel et al. [11] examined children with hearing loss in three different age groups (4.5–6.5 years, 8–10 years, and 12.5–14.5 years) using the balance subtest of the BOTMP in order to determine age-related changes in balance ability. The results of the comparison with the normative data showed that the balance ability of children with hearing loss improves until they reach approximately 10 years of age, after which any existing deficits persist. According to a study by Brunt and Broadhead [9], the balance ability of children with hearing loss improves with age but remains lower than that of NH children at the age of 7–14 years. On the other hand, studies of postural stability in patients with vestibular dysfunction have shown that the degree of postural sway during quiet stance is normal in conditions under which either visual or somatosensory input is enabled. In contrast, they have a hard time maintaining postural stability when both visual and somatosensory inputs are inadequate [12,13]. Empirical research suggests that older children with hearing impairment have relatively functional postural stability as a result of the contribution of adaptive sensory compensation [5,12,14]. According to a study by Kaga [5], vestibular loss in children with hearing loss is nearly completely compensated for by the contribution of the visual and somatosensory systems, and by the plasticity of the CNS, by 10 years of age. Suarez et al. [6] examined postural control in children with hearing impairment at 8–11 years of age under two different sensory conditions: standing on a firm surface with eyes open (condition 1) and standing on a foam surface with eyes closed (condition 2). The children with hearing impairment found it difficult controlling their upright posture in condition 2, where visual information was removed and somatosensory information was modified. Recent studies have focused on age-related changes in the postural development of children with hearing impairment, but their findings remain equivocal. In addition, few previous studies have examined sensory compensation of children with hearing impairment and compared this in age-matched NH children. The study presented here was thus designed to elucidate the agerelated changes in single-limb standing balance and sensory compensation for maintaining postural stability in altered sensory conditions in PD children. The results are compared with those of age-matched NH children. 2. Method 2.1. Subjects The study involved 57 PD children aged 4–14 years of age and 57 age-matched NH children (Table 1). The children were recruited from two local elementary schools, a middle school, and three schools for the deaf. Each group was subdivided according to age: group 1, 4–6 years; group 2, 7–9 years; and group 3, 12–14 years. Inclusion criteria for the PD group included a hearing loss greater
Table 1 Characteristics of the subjects (n = 114). Hearing ability
Age group
Children with deafness (n1 = 57)
4–6 years 7–9 years 12–14 years 4–6 years 7–9 years 12–14 years
Children with normal hearing (n2 = 57)
Gender Male
Female
7 12 14 8 12 12
11 7 6 10 7 8
than 70 dB; we did not determine the etiology of the hearing loss. Exclusion criteria for all subjects included any neuromuscular or musculoskeletal condition, uncorrected visual disability, and learning disability as identified from school records. The subjects and their parents were informed about the purpose, procedures, and applications of this study, and parental agreement for their children to participate was obtained. 2.2. Experimental equipment The equipment used included a silent stopwatch that can measure centesimal units, eye bandages, and 5-cm-thick foam sponges. 2.2.1. Single-limb standing test (SLS) The single-limb standing test is a commonly used clinical tool for the measurement of standing balance. It assesses postural stability in a static standing position by measuring the time (in seconds) a subject can maintain the single-limb standing position. Atwater et al. [15] have shown that the single-limb standing test has good interrater reliability (r = 0.87–0.99) and fair-to-good test– retest reliability (r = 0.59–1.00) in both the eyes open and eyes closed conditions. 2.3. Procedure We administered a static standing balance test in a quiet classroom in the schools. Before testing, each child was required to kick a ball to define his or her dominant leg, which was used for the balance test. Static standing balance was assessed with the singlelimb standing test under four different sensory conditions: standing on a firm surface with eyes open (condition 1), standing on a firm surface with eyes closed and covered (condition 2), standing on a foam surface with eyes open (condition 3), and standing on a foam surface with eyes closed and covered (condition 4). The test was performed twice for each condition and the better performance was recorded. The children were allowed to rest for 1 min between tests to prevent muscle fatigue. The four conditions were administered in a random order by drawing lots. All directions were explained to each subject via total communication, which involves speech, sign language, body language, and demonstration. The subjects were instructed to stand on one leg for as long as possible but for a maximum of 60 s for each trial. They were barefoot and positioned 2 m from a wall upon which a visual target had been placed at their eye level. When standing with eyes open during the test (conditions 1 and 3), the subjects were instructed to look at the target. When standing with eyes closed (conditions 2 and 4), an eye bandage was used to cover the subject’s eyes in order to prevent them from furtively opening them. The subjects were instructed to place their hands on their hips, raise their nondominant leg behind them with their knee bent at 908 and shin parallel to the floor, and to look at the target. For all conditions, timing was started as soon as the angle of knee became 908 with the shin parallel to the floor. Timing was stopped when the
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subjects touched the raised foot to the floor, took their hands off of their hips, or shifted the supporting foot from the starting position. Timing was also stopped if the subject continued to hook the raised leg behind the support leg after two warnings, or failed to keep the raised leg lifted to at least the mid-range of knee flexion. 2.4. Statistical analysis The primary analysis was repeated-measures analysis of variance (ANOVA), with age as the between-subjects factor and condition as the within-subject factor. Eight separate one-way ANOVAs were then used to determine the age-related changes of single-limb standing balance in PD and NH children in altered sensory conditions. Where the one-way ANOVA showed a significant difference, Bonferroni’s adjustment was used to identify where specific differences occurred. Two-way ANOVAs (age hearing ability) by condition were used to determine if there were differences in single-limb standing balance depending on the hearing ability. Independent t-tests were also used to verify if there were differences in the mean single-limb standing time between the PD and NH children in each age group. The SPSS statistical package was used to analyze differences in single-limb standing balance in PD and NH. Hypothesis testing was carried out with a = 0.05. 3. Results 3.1. General single-limb standing balance Table 2 lists the mean time for maintaining postural stability in the single-limb standing balance test. Single-limb standing balance in both the PD and NH group was significantly different depending on age (Tables 3, 5 and 7). In general, the PD group demonstrated significantly lower single-limb standing balance than the NH group (Fig. 1) (Table 3).
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3.2. Age-related changes in single-limb standing balance Repeated-measures ANOVAs showed significant main effects for age and condition in both the PD and NH groups. There was an interaction, however, between age and condition in the PD group, but not in the NH group (Fig. 2) (Tables 4–7), which indicates that the age-related changes in single-limb standing balance in the PD group were affected by the sensory conditions, in contrast with those in the NH group, which were not affected by the sensory conditions (Fig. 3). The independent t-test, which was used to compare the mean single-limb standing time of the PD children with the age-matched NH children, indicated a significant difference in single-limb standing balance within each age group, depending on the condition and age. In age group 1, there were significant differences between the PD and NH children under all conditions. These differences diminished with age, however, except for condition 2, where the difference between both groups persisted regardless of age (Fig. 1). 3.3. Single-limb standing balance under specific sensory condition The single-limb standing balance of the PD children was significantly lower than that of the NH children. In specific sensory conditions, however, where visual information was enabled, the single-limb standing balance of the PD group improved with age and reached a level similar to that seen in the NH group. Fig. 3 shows the age-related changes in single-limb standing balance under specific sensory conditions. In condition 1, the mean time for the PD group significantly increased with age, but an increase in the mean time for the NH group was only observed in a comparison between age group 3 (12–14 years) and age group 1 (4–6 years). In condition 2, both the PD and NH groups showed a significant difference between age groups 1 and 3 only. In condition 3, significant increases were found between age groups 1 and 2, and age groups 1 and 3 among the PD
Table 2 Time for maintaining one-leg standing balance by age group and sensory condition (unit: seconds). Age group (years)
Condition Condition Condition Condition
1 2 3 4
PD group (n1 = 57)
NH group (n2 = 57)
4–6 (n = 18)
7–9 (n = 19)
12–14 (n = 20)
4–6 (n = 18)
7–9 (n = 19)
12–14 (n = 20)
4.33 4.66a 1.89 1.38 2.46 1.91 1.23 0.59
21.61 7.28 4.26 4.14 17.33 9.03 3.07 2.25
37.16 17.96 4.89 3.82 28.61 18.12 4.32 7.12
37.55 21.11 9.19 7.29 33.62 21.60 4.96 4.67
42.99 9.63 10.06 9.63 34.23 20.36 5.43 4.13
53.35 12.18 18.98 16.38 45.93 18.81 9.98 13.08
PD: profoundly deaf; NH: normal hearing. Condition 1: eyes open, firm surface; condition 2: eyes closed, firm surface Condition 3: eyes open, foam surface; condition 4: eyes closed, foam surface. a Mean SD. Table 3 Summary for the two-way ANOVA by condition.
Condition 1
Condition 2
Condition 3
Condition 4
Age Hearing ability Age hearing ability Age Hearing ability Age hearing ability Age Hearing ability Age hearing ability Age Hearing ability Age hearing ability
Type III sum of squares
df
Mean square
F
p
11253.022 15843.688 1426.976 852.650 2336.673 382.464 7150.557 13512.347 1215.820 335.303 436.461 53.719
2 1 2 2 1 2 2 1 2 2 1 2
5625.511 15843.688 713.488 426.325 2336.673 191.731 3575.278 13512.347 607.910 167.651 436.461 26.190
20.583 57.960 2.610 5.556 30.453 2.492 11.053 41.773 1.879 3.630 9.449 .581
.000** .000** .078 .005** .000** .087 .000** .000** .158 .030* .003** .561
Age and hearing ability were the main factors affecting single-limb standing balance under four different conditions in children. * p < 0.05. ** p < 0.01.
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Fig. 1. Comparison using the independent t-test of the mean time for maintaining single-limb standing between PD and NH children (*p < 0.05, **p < 0.01). The deficit in the PD children’s single-limb standing balance dwindled with age in conditions 1 and 3, in which visual information was enabled. In condition 2, however, in which visual input was removed, the deficit in the PD children’s single-limb standing balance persisted. Condition 1: eyes open, firm surface; condition 2: eyes closed, firm surface; condition 3: eyes open, foam surface; condition 4: eyes closed, foam surface. Age group 1: 4–6 years; age group 2: 7–9 years; age group 3: 12–14 years.
children; no significant differences were found in the NH children. In condition 4, both the PD and NH groups showed no statistically significant differences between any age group. 4. Discussion Vision is important during quiet stance, but it is not absolutely necessary to maintain postural stability because not only visual but also somatosensory and vestibular inputs all influence quiet stance postural control. However, there were significant agerelated changes among the PD children in both condition 1, where visual information was enabled, and condition 2, where visual input was obscured, although the improvement with age was much greater in condition 1 than in condition 2. In contrast, NH children showed a similar result in the comparison of both conditions. This indicates that the single-limb standing balance of children who are PD improves as a result of the provision of visual information rather than somatosensory inputs, and this dependence become essential with age. In addition, our finding that the improvement of single-limb standing balance seen under condition 1 was continuous until age group 3 (12–14 years) is
inconsistent with the finding of Kaga’s study [5] that vestibular dysfunction in children with hearing impairment is compensated for by visual and somatosensory inputs by 10 years of age. The PD children showed obvious age-related improvements in single-limb standing balance under condition 3, where visual information was enabled and the supporting surface was perturbed. This differs from the observations in NH children, who demonstrated no significant differences with age, indicating that PD children compensate for their postural instability using somatosensory and visual information. Somatosensory information is the most important for maintaining standing balance on a perturbed supporting surface [4], but a difficult balance task is associated with a higher reliance on visual cues [16]. Moreover, vestibular responses to support-surface perturbation appear to be much smaller than those of somatosensory input [17]. Thus, under condition 3, the PD children might have compensated for their postural instability by using visual and somatosensory information. When children were examined under condition 4, no agerelated changes in single-limb standing balance were seen in either the PD or NH groups. Since the information provided by the
Fig. 2. Comparisons between sensory conditions for maintaining single-limb standing in each age group. This figure shows an interaction between age and condition in the PD group but not in the NH group. Age group 1: 4–6 years; age group 2: 7–9 years; age group 3: 12–14 years. Condition 1: eyes open, firm surface; condition 2: eyes closed, firm surface; condition 3: eyes open, foam surface; condition 4: eyes closed, foam surface.
M.-h. An et al. / International Journal of Pediatric Otorhinolaryngology 73 (2009) 1539–1544 Table 4 Multivariate tests performed on the data of mean time of maintaining single-limb standing in PD children. Effect
Value
F
Hypothesis df
Error df
p
Condition Condition age
0.357 0.541
31.277 6.235
3.000 6.000
52.000 104.000
0.000 0.000
The PD children’s single-limb standing balance was affected by condition and age, and there was an interaction between the two.
Table 5 Between-subject tests of the effect on the mean time for maintaining single-limb standing in PD children.
Age
Type III sum of squares
df
Mean square
F
p
2509.874
2
1254.937
21.746
0.000
Table 6 Multivariate tests performed on the data of mean time of maintaining single-limb standing in NH children. Effect
Value
F
Hypothesis df
Error df
p
Condition Condition age
0.173 0.907
83.100 0.872
3.000 6.000
52.000 104.000
0.000 0.518
The NH children’s single-limb standing balance was affected by condition and age, and there was no interaction between the two.
Table 7 Between-subject tests of the effect on the mean time for maintaining single-limb standing in NH children.
Age
Type III sum of squares
df
Mean square
F
p
1273.932
2
636.966
4.831
0.000
vestibular system, which is inertial and gravitational, is not affected by the environmental context, vestibular information is important for resolving the intersensory conflict [13,18]. When children maintain their single-limb standing balance under eyes closed, compliant-foot-support conditions, such as condition 4, the
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vestibular inputs are essential in providing an absolute reference for postural control. However, vestibular function develops more slowly than do visual and somatosensory functions [13,19]. Hirabayashi and Iwasaki [18] studied the development of sensory organization on postural control under various sensory conditions using computerized dynamic posturography. They measured the subjects’ sway, calculated from the maximum displacement of the center of gravity, while they (112 children aged 3–15 years and 26 adults aged 20–60 years) stood under 6 different sensory conditions. Their results show that vestibular function had not reached the adult level even at the age of 14–15 years. Since all children who participated in the present study were under 15 years of age, it is likely that their vestibular function had thus not yet matured. This is the most likely reason why no age-related changes in single-limb standing balance were observed in either the PD or NH children. Our results can be explained by the concept of sensory weighting, which asserts that people maintain their postural stability based on the relative accuracy of sensory input reporting the body’s position and movement in space [13,20]. When a sense provides inaccurate information, the weight given to that sense is reduced, while the weight of other senses that continue to provide more accurate information is increased [4]. Based on the concept of sensory weighting, PD children who might also have vestibular dysfunction might be more reliant on visual and somatosensory information, which is putatively more reliable than vestibular information. In the present study, when visual information was enabled but somatosensory input was inaccurate, as in condition 3, single-limb standing balance in the PD children improved with age and even reached at levels similar to those of the NH children. However, when visual information was enabled and somatosensory input was accurate, as in condition 1, single-limb standing balance in PD children increased with age but remained lower than that of the NH children. Furthermore, when visual information was unable but somatosensory input was accurate, as in condition 2, single-limb standing balance improved just a little. These findings indicate that although children with hearing impairment do compensate for their vestibular dysfunction with visual and somatosensory inputs, the dependence on visual input is greater than on somatosensory input.
Fig. 3. Between age group comparisons using eight separate one-way ANOVAs with Bonferroni’s adjustment. Mean time in each age group for maintaining single-limb standing under four sensory conditions (*p < 0.05, **p < 0.01). The older PD children’s single-limb standing balance was significantly better than that of the younger PD children under certain sensory conditions where visual information was enabled. Age group 1: 4–6 years; age group 2: 7–9 years; age group 3: 12–14 years. Condition 1: eyes open, firm surface; condition 2: eyes closed, firm surface; condition 3: eyes open, foam surface; condition 4: eyes closed, foam surface.
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In summary, the single-limb standing balance of older PD children improves by adaptive sensory compensation, in contrast to younger PD children, who show significant deficits in single-limb standing balance. However, the dependence upon visual input for maintaining postural stability is higher than on somatosensory input. If PD children continuously rely on vision for postural stability, they might have a hard time maintaining postural stability under conditions in which visual input is insufficient or has been removed. Parents and teachers should therefore be aware of possibly dangerous situations for such children, such as walking in the dark, and should work to prevent them from encountering this type of situation unattended. In addition, it might be useful for deaf children to train with the intention of developing their somatosensory functions. This developmental study was completed using the single-limb standing balance test, which provides a quantitative measure of postural stability. Although this clinical tool is reliable, using other accurate assessment equipment together might provide even more reliable and accurate data. In addition, we were unable to assess the true age-related changes of single-limb standing balance under condition 4 due to the limited age range of 4–14 years used in this study. Further research should examine a wider range of ages with greater numbers of children to more completely define the agerelated changes of postural control in PD children. 5. Conclusion The objective of this study was to determine any age-related changes in single-limb standing balance and sensory compensation in PD and NH children aged 4–14 years under normal and altered sensory conditions. The results of the single-limb standing balance testing demonstrated that postural stability in PD children improves with age under the specific sensory conditions used in our testing. The method of improvement was adaptive sensory compensation, which includes both visual and somatosensory inputs. However, since visual dependency was much higher than somatosensory dependency in the PD children, it is suggested that PD children should enhance their somatosensory functions in order to better maintain their postural stability.
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