Acta Oto-Laryngologica. 2014; 134: 672–678
ORIGINAL ARTICLE
Relationship between acquisition of motor function and vestibular function in children with bilateral severe hearing loss
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TAKESHI MASUDA1,2 & KIMITAKA KAGA1 1
National Institute of Sensory Organs, Tokyo and 2Otolaryngology-Head and Neck Surgery, Nihon University School of Medicine, Tokyo, Japan
Abstract Conclusions: When vestibular function is reduced in the rotational chair test in children with severe hearing loss, the vestibular function may be acquired later due to maturing vestibular sensory cells and vestibular nerve of the inner ear along with physical growth. Objectives: To examine the relationship between acquisition of motor function and vestibular function in children with bilateral severe hearing loss. Methods: A total of 97 children under 4 years old with hearing loss defined as a hearing threshold of both ears greater than 80 dB were included in this study. For evaluation of vestibular function, a damped-rotational chair test was performed and the horizontal nystagmus was recorded using electronystagmography (ENG). Results: Head control and independent walking were delayed in 28 of 97 children with severe hearing loss. Reduced response to the rotational chair test was observed in 16 of 97 children (16.5%), with 11 of these children having inner ear anomalies and reduced vestibular function. Of the 10 children who were followed up by the rotational chair test, 2 children with idiopathic congenital hearing loss without inner ear anomalies (100%) and 6 of 8 children with bilateral inner ear anomalies (75%) showed more obvious nystagmus during rotation compared with the initial examination.
Keywords: Inner ear malformation, rotational chair test
Introduction The developmental neurology of balance impairment in infants and children began from the observation of postural reflex of infants and children. AndrésThomas reported that the presence or absence of labyrinthine righting reflex is important in diagnosing pediatric neurological diseases, and he clarified the characteristics of posture changes and development of the newborn in the mid-20th century. Rapin noticed that a delay in motor development in infancy was often reported in students at the school for hearing impaired children and reported this in a retrospective study in 1974 [1]. Kaga et al. in 1981 examined the vestibulo-ocular reflex (VOR) quantitatively in children with severe hearing loss using a rotational chair and demonstrated that head control and independent walking are delayed when the VOR is lacking [2]. Currently, inner ear morphology can be
observed in detail due to the development of high-resolution CT, and inner ear malformations and narrowing of the internal auditory canal can be revealed. However, there have been no reports that follow up on changes of the VOR due to development. Therefore, we evaluated the vestibular function of children with bilateral severe hearing loss using a rotational chair test. In addition, we performed a follow-up study on the relationship between vestibular function and motor development for which head control and independent walking were used as indicators of motor development. Material and methods Patients A total of 97 children under 4 years old with a hearing threshold for both ears greater than 80 dB and who
Correspondence: Takeshi Masuda, Otolaryngology-Head and Neck Surgery, Nihon University School of Medicine, Tokyo, Japan. E-mail: [email protected]
(Received 9 December 2013; accepted 24 January 2014) ISSN 0001-6489 print/ISSN 1651-2251 online 2014 Informa Healthcare DOI: 10.3109/00016489.2014.890290
Acta Otolaryngol Downloaded from informahealthcare.com by University of Laval on 07/05/14 For personal use only.
Acquisition of vestibular function in children visited the Tokyo Medical Center Hospital for infants and children with hearing loss and language disorders during the 5 years between June 2008 and October 2013 were studied. None of the children had had cochlear implant surgery before the initial examination. Their ages ranged from 3 months to 37 months, with an average age of 23.1 months and a median age of 22.5 months. Assessment of hearing was determined comprehensively using the auditory steady state response (ASSR), auditory brainstem response (ABR) test, and conditioned orientation reflex (COR) to measure the hearing threshold. We use not only ABR but ASSR and COR when a child has the possibility of low tone hearing. Genetic testing related to hearing was conducted in a small number of the patients whose parents requested it and the results of the genetic testing were not included in the evaluation. Inner ear malformations were classified according to the classification by Sennaroglu and Saatci [3]. Head control (the state in which a motion of the head is controllable by itself) and independent walking (the state in which there is no support and the child can walk by him or herself) were used as indicators of motor development. Based on the results of an infant and children physical development survey report in 2010 conducted by the Ministry of Health, Labour and Welfare of Japan, a delay in motor development was determined when head control was later than 5 months and independent walking was later than 14 months, which are the 97th percentile values. Head control and independent walking were checked using the mother-and-baby notebook for medical and welfare records, the notebook handed out by local public organizations in Japan. We followed up the children that were under 6 months old for 1 year or more. In cases of premature birth, the children were evaluated using a corrected age.
673
the horizontal direction. An electrical calibration with 100 mV was used for calibration of eye movement. The number of beats of nystagmus during rotation and duration of time for nystagmus were measured and the average values of the left and right rotations were obtained. When both were less than 50% of the age control data of Kaga et al. [2], the vestibular function was determined to be reduced. Results The causes of hearing loss in the 97 children with bilateral severe hearing loss were idiopathic congenital hearing loss in 66 children, bilateral inner ear malformation in 12 children, cytomegalovirus (CMV) infection in 5 children, auditory neuropathy in 4 children, symptomatic hearing impairment in 3 children, meningitis in 3 children, large vestibular aqueduct syndrome in 2 children, deaf and blind in 1 child, and hyperbilirubinemia in 1 child (Table I). Motor development was delayed in 28 of 97 children (28.9%). Of these 28 children, 16 (57.1%) showed a reduced response to the rotational chair test. Of the 28 children who showed a delay in motor development, the causes were inner ear malformation in 12 children, idiopathic congenital hearing loss in 10 children, symptomatic hearing impairment in 2 children, CMV infection in 2 children, deaf and blind in 1 child, and large vestibular aqueduct syndrome in 1 child. The response to the rotational chair test was reduced in 16 of 97 children (16.5%). All of these 16 children showed delayed motor development. Of the 16 children who showed reduced response to the rotational chair test, the causes were inner ear malformation in 11 children, idiopathic congenital hearing loss in 4 children, and deaf and blind in 1 child (Figure 1). The follow-up examination performed in two of four children with idiopathic congenital hearing loss
Rotational chair test Table I. Causes of hearing loss and average ages of the children.
Earth-vertical axis rotation (EVAR) was used for the rotational chair test. A damped-rotational chair test similar to the protocol of Kaga et al. [2] was performed using a computer-controlled rotational chair (type S-II; Nagashima Co. Ltd, Tokyo, Japan). For the safety of the children, a parent sat on the rotational chair first and then held the child on their lap during the rotational chair test. The test was performed in the dark to reduce the influence of the visual suppression and the velocity was decelerated by 4 /s from the initial velocity of 160 /s. Right rotation was performed first, followed by left rotation after a 5 min interval. Nystagmus was recorded by electronystagmography (ENG). The electrodes were placed near the lateral canthus of both eyes to record the eye movement in
No. of patients
Average age
Idiopathic congenital hearing loss
66
2 years 0 months
Bilateral inner ear malformation
12
1 year 10 months
Cytomegalovirus infection
5
2 years 6 months
Auditory neuropathy
4
1 year 1 month
Symptomatic hearing impairment
3
1 year 5 months
Meningitis
3
1 year 4 months
Large vestibular aqueduct syndrome
2
1 year 8 months
Hyperbilirubinemia
1
2 years 1 month
1
2 years 7 months
97
1 year 11 months
Cause of hearing impairment
Deaf and blind Total
674
T. Masuda & K. Kaga Per-rotatory nystagmus
Motor development Normal: 69
Normal response: 69
97 patients
Normal response: 12 Delay: 28
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Bilateral inner ear malformation: 12 Idiopathic congenital hearing loss: 10 Symptomatic hearing impairment: 2 Cytomegalovirus infection: 2 Deaf and blind: 1 Large vestibular aqueduct: 1
Poor response: 16 Bilateral inner ear malformation: 11 Idiopathic congenital hearing loss: 4 Deaf and blind: 1
Figure 1. Results of motor development and nystagmus during rotation. Among 97 children, 16 of 28 who showed a delay in motor development also showed a reduced response to the rotation test. Motor development was normal in 69 children, and all showed a normal response to the rotation test.
whose vestibular function was reduced at the initial examination showed that distinct nystagmus began to appear in all children (Table II). The follow-up examination of the eight children with inner ear malformation showed that distinct nystagmus began to appear compared with the initial examination in six children (Table III). The number of beats of nystagmus during rotation and the duration of time for nystagmus were plotted through the time course for 10 children who were followed up, as described above, and compared with the control data of Kaga et al. [2]. The number of beats of nystagmus increased with age in 8 of the 10 children, but not in the other 2 children (nos 4 and 7). Despite the fact that children nos 3 and 8 showed no response in the initial examination, they began to show a better response than the control data (Figure 2). The duration of time for nystagmus was increased with age in eight children, but not in nos 4 and 7. Seven children (nos 1, 3, 5, 6, 8, 9, and 10) developed a good response that exceeded the control data (Figure 3). Discussion Motor development in children with congenital severe hearing loss is often delayed. A reason for delayed
head control and independent walking may be the loss of muscle from the vestibule and, thus, sufficient tension cannot be maintained [4]. In children with severe hearing loss, not only hearing, but also the vestibular nerve and vestibular sensory cells may have abnormalities that cause a delay in motor development [5]. This study also showed that motor development, such as head control and independent walking, was delayed in 28 of 97 children with severe hearing loss. Some reports have evaluated vestibular function in children [6–8], but it is difficult to perform vestibular function testing in infants. However, it is possible to evaluate vestibular function quantitatively even in infants from whom cooperation is not obtained, by using a damped-rotational chair test. Eviatar et al. [9] conducted a caloric test and rotation test in 276 infants aged from 1 day to 1 year old and divided into four groups by every 3 months after birth. Nystagmus was more difficult to elicit in the younger age children in the caloric test, whereas it appeared regardless of age in the rotation test. As evidenced by a canal plugging experiment in monkeys, the rotation test is one of the most stimulating tests among the vestibular function tests because it applies stimulus to the semicircular canals and otolith organs in both ears [10]. Therefore, it can detect the response even when the VOR is very weak.
Table II. Follow-up results of the damped-rotational chair test in children with normal inner ear morphology. Child no. 1
Age
Disease
1 year 10 months
Idiopathic congenital hearing loss
3 years 10 months 2
1 year 10 months 3 years 1 month
Idiopathic congenital hearing loss
Time duration (s)
No. of beats
Head control
Independent walking
0
0
5 months
1 year 10 months
32.5
16
2 years 7 months, right
12 months
1 year 10 months
–
2.5 13
2.5
CI
13
In two children with idiopathic hearing loss without morphological anomalies in the inner ear, a distinct vestibulo-ocular reflex (VOR) compared with the initial examination appeared. CI, age when cochlear implant surgery was performed.
Acquisition of vestibular function in children
675
Table III. Follow-up results of the damped-rotational chair test in children with inner ear malformation. No. 3
Age 6 months
Type of cochlear anomaly Bilateral IP-II
Type of vestibular anomaly
Time duration (s)
No. of beats
Head control
0
0
6 months
37
40.5
1 year 4 months
2 years 0 months, left
10 months
1 year 10 months
2 years 10 months, left
6 months
1 year 6 months
1 year, 10 months, right
6 months
1 year 1 month
2 years 1 month, left
8 months
1 year 10 months
3 years 10 months, left
6 months
1 year 10 months
2 years 4 months, right
6 months
1 year 6 months
2 years 8 months, right
6 months
1 year 4 months
3 years 4 months, right
Bilateral normal
1 year 10 months 4
6 months
Bilateral IP-II
Bilateral vestibular hypoplasia
0
0
0
0
1 year 11 months
0
0
3 years 2 months
2
2
1 year 4 months
5
6 months
6
9 months 1 year 2 months
Bilateral common cavity
Bilateral common cavity
Left IP-II, right IP-I
Bilateral normal
7
1 year 9 months 3 years 2 months
0
0
31.5
28.5
0
0
9.5
2 years 0 months
28 Left IP-I, right Michel
Left normal, right Michel
12.5
2 years 3 months
Left IP-I, right cochlear hypoplasia
Left normal, right vestibular hypoplasia
3 years 7 months 9
2 years 6 months 3 years 5 months
Bilateral common cavity
Bilateral common cavity
Bilateral IP-I
Bilateral normal
4 years 9 months 10
3 years 3 months
8
7.5
7
0
0
29.5
34
3.5
3.5
0
0
39
28
37
CI
21
3.5
6
5 years 7 months
11
2.5
3 years 5 months 8
3.5 22
In six of eight children (75%) with inner ear malformation, a distinct vestibulo-ocular reflex (VOR) appeared compared with the initial examination. CI, age when cochlear implant surgery was performed; IP-I, incomplete partition type I; IP-II, incomplete partition type II [3].
Number of beats 45 No.3 40 No.8
35 Number of times
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4 years 7 months
Independent walking
Control
30 No.5 25
No.9 No.10
No.6
20
No.1 No.2
15 10
No.7
5 No.4
0 0
6m
1y 1y6m 2y 2y6m 3y 3y6m 4y 4y6m 5y 5y6m 6y (age)
Figure 2. The time course and the number of beats of nystagmus during rotation of all 10 children who had a follow-up examination. Except for nos 4 and 7, eight children showed an increase with growth in the number of beats of nystagmus during rotation. In particular, nos 3 and 8 began to show a better response than the control data despite no reaction in the initial examination. The dashed line indicates control data from Kaga et al. [2].
676
T. Masuda & K. Kaga Duration of time for nystagmus 45 No.9
40
No.10
No.3
35
No.1 No.5
(sec)
30
No.6
No.8
25 Control
20 15
No.7
No.2
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10 5 No.4 0 0
6m
1y 1y6m 2y 2y6m 3y 3y6m 4y 4y6m 5y 5y6m 6y (age)
Figure 3. The time course and duration of time for nystagmus of all 10 children who had a follow-up examination. Similar to Figure 2, 8 of the 10 children (except nos 4 and 7) showed an increase with growth in the duration of time for nystagmus. In particular, seven children (nos 1, 3, 5, 6, 8, 9, and 10) showed a good response that exceeded the control data. The dashed line indicates control data from Kaga et al. [2].
Since 2008 in our facility, the damped-rotational chair test has been performed and vestibular function, along with motor development, has been evaluated before cochlear implant surgery. In the results, 16 of 97 children showed reduced response to the dampedrotational chair test and all of these 16 children showed delayed motor development. In particular, 11 of 12 children with bilateral inner ear malformation showed delayed motor development (Figure 1). The follow-up examination was carried out for 10 of 16 children with reduced response to the initial rotational chair test. Of these 10 children, idiopathic congenital hearing loss was observed in 2 children and inner ear malformation was observed in 8 children. As a result, both the two children with idiopathic congenital hearing loss (100%) and six of eight children with inner ear malformation (75%) began to show a distinct VOR compared with the initial examination. The result of the rotational chair test was normal in 12 of 28 children who had delayed motor development. A rotational chair test stimulates both the ears. Therefore, the stimulus is stronger than a caloric test 1.Vestibular nerve
or VEMP, and cannot detect a laterality and slight reduction of VOR. When using a caloric test or VEMP in these 12 children, abnormalities may have been detected. Jin et al. [11] performed the VEMP test in seven children with inner ear malformation after cochlear implant surgery and evaluated the presence or absence of the response. All children showed VEMP responses when the power of the cochlear implant was turned on. This result suggests that the vestibular nerve is present even if there is an inner ear malformation. The reason why the VOR did not appear in the initial examination, but began to appear in the followup in this study, was considered separately in the presence or absence of inner ear malformation. In order for the VOR to appear in the rotational chair test when there are no morphological anomalies in the inner ear, the cupula must function as a sensor and the vestibular nerve must transmit signals into the brainstem. According to current knowledge of embryology, the membranous labyrinth is completed in viviparous 9 months. However, the vestibular sensory
2.Sensory neuron (Cupula)
3.Vestibular nerve & Cupula
Vestibular nerve
Cochlear nerve
Sensory neuron (Cupula)
Figure 4. Acquisition of the vestibulo-ocular reflex (VOR) in children with normal inner ear morphology. (1) Development of the vestibular nerve. (2) Maturation of balance sensory cells (cupula). (3) Both (1) and (2).
Acquisition of vestibular function in children 1.Vestibular nerve
2.Sensory neuron (Macula) Sensory neuron (Macula) Vestibular nerve
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3.Vestibular nerve & sensory neuron
Cochlear nerve
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Figure 5. Acquisition of the vestibulo-ocular reflex (VOR) in children with inner ear malformation. (1) Development of vestibular nerve. (2) Maturation of the macula (vestibular sensory cells). (3) Both (1) and (2).
neurons are completed at the 23 weeks stage. Furthermore, the vestibular nerve is completed at 5 months, although the form of the membranous labyrinth is in the same state as at 6 weeks of viviparous time in common cavity malformation, after which myelinization of the vestibular nerve and maturation of the sensory cells take place [12,13]. Figures 4 and 5 are drawn from current embryological knowledge. The appearance of the VOR with age in children with no inner ear anomalies may be due to maturation of the vestibular nerve, maturation of balance sensory cells, or both (Figure 4). In regard to cases with inner ear malformations, common cavity malformations were examined as an example. In EVAR, which was performed in this study, the cupula of the lateral semicircular canals was stimulated primarily in cases with normal inner ear morphology. However, for children with an inner ear malformation, since the fixed axis does not exist in the vestibular organs, the otolith organs are stimulated similar to when OVAR (off-vertical axis rotation) stimulus is used. The appearance of the VOR with age in children with inner ear malformation may be due to maturation of the vestibular nerve, maturation of the macula (vestibular sensory cells), or both (Figure 5). Children with inner ear malformation show a delay in motor development in their infancy, but acquire vestibular compensation from the central nervous system (CNS) or muscle tone due to the reflex from the vestibular labyrinth and growth. By junior high or high school stage, the children can perform most exercises without problems [4]. The present study reconfirmed that head control and independent walking are delayed if the acquisition of the VOR is insufficient. However, the VOR may be acquired with growth even if it is reduced during early childhood. It is necessary to accurately evaluate vestibular function in children to determine the proper rehabilitation strategy [14]. This study does not clarify completely the relationship between the vestibular function and motor development in children with severe hearing loss. Further studies, including analysis of genetic abnormalities and mental retardation, as well as multiple disabilities in children are required.
Conclusions (1) Twenty-eight of 97 children with bilateral severe hearing loss showed a delay in head control or independent walking. (2) The damped-rotational chair test was performed in 97 children younger than 4 years old with severe hearing loss. Sixteen children (17%) showed no response or severely reduced response. Of those, 11 of 12 children (91.7%) with inner ear malformation showed reduced vestibular function. (3) Of the 10 children who were followed up with the rotational chair test, the VOR began to appear with growth in the 2 children without inner ear malformation (100%) and in 6 of 8 children with bilateral inner ear malformation (75%). (4) These results suggest that vestibular function may be acquired due to the maturation of vestibular sensory cells and vestibular nerve in the inner ear along with growth in children with severe hearing loss and reduced vestibular function.
Acknowledgment The authors thank Mrs Yakushimaru for her clinical examination work. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References [1] Lapin I. Hypoactive labyrinths and motor development. Clin Pediatr 1974;13:922–37. [2] Kaga K, Suzuki JI, Marsh RR, Tanaka Y. Influence of labyrinthine hypoactivity on gross motor development of infants. Ann NY Acad Sci 1981;374:412–20. [3] Sennaroglu L, Saatci I. A new classification for cochleovestibular malformations. Laryngoscope 2002;112:2230–41. [4] Kaga K. Vestibular compensation in infants and children with congenital and acquired vestibular loss in both ears. Int J Pediatr Otorhinolaryngol 1999;49:215–24. [5] Kaga K, Shinjo Y, Jin Y, Takegoshi H. Vestibular failure in children with congenital deafness. Int J Audiol 2008;47:590–9.
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[6] Staller SJ, Goin DW, Hildebrandt M. Pediatric vestibular evaluation with harmonic acceleration. Otolaryngol Head Neck Surg 1986;95:471–6. [7] Shinjo Y, Jin Y, Kaga K. Assessment of vestibular function of infants and children with congenital and acquired deafness using the ice-water caloric test, rotational chair test and vestibular-evoked myogenic potential recording. Acta Otolaryngol 2007;127:736–47. [8] De Kegel A, Maes L, Baetens T, Dhooge I, Van Waelvelde H. The influence of a vestibular dysfunction on the motor development of hearing-impaired children. Laryngoscope 2012;122:2837–43. [9] Eviatar L, Miranda S, Eviatar A, Freeman K, Borkowski M. Development of nystagmus in response to vestibular stimulation in infants. Ann Neurol 1979;5: 508–14.
[10] Cohen B, Suzuki JI, Raphan T. Role of the otolith organs in generation of horizontal nystagmus: effects of selective labyrinthine lesions. Brain Res 1983;276:159–64. [11] Jin Y, Shinjo Y, Akamatsu Y, Yamasoba T, Kaga K. Vestibular evoked myogenic potentials of children with inner ear malformations before and after cochlear implantation. Acta Otolaryngol 2009;129:1198–205. [12] Moore KL, Persaud TVN, Torchia MG. 2012. Development of peripheral nervous system. In The developing human: clinically oriented embryology. 9th edition. Philadelphia: Elsevier Saunders. p 423–5. [13] Moore KL, Persaud TVN, Torchia MG. 2012. Development of ears. In The developing human: clinically oriented embryology. 9th edition. Philadelphia: Elsevier Saunders. p 441–9. [14] Nandi R, Luxon LM. Development and assessment of the vestibular system. Int J Audiol 2008;47:566–77.
ORIGINAL ARTICLE
Relationship between acquisition of motor function and vestibular function in children with bilateral severe hearing loss
Acta Otolaryngol Downloaded from informahealthcare.com by University of Laval on 07/05/14 For personal use only.
TAKESHI MASUDA1,2 & KIMITAKA KAGA1 1
National Institute of Sensory Organs, Tokyo and 2Otolaryngology-Head and Neck Surgery, Nihon University School of Medicine, Tokyo, Japan
Abstract Conclusions: When vestibular function is reduced in the rotational chair test in children with severe hearing loss, the vestibular function may be acquired later due to maturing vestibular sensory cells and vestibular nerve of the inner ear along with physical growth. Objectives: To examine the relationship between acquisition of motor function and vestibular function in children with bilateral severe hearing loss. Methods: A total of 97 children under 4 years old with hearing loss defined as a hearing threshold of both ears greater than 80 dB were included in this study. For evaluation of vestibular function, a damped-rotational chair test was performed and the horizontal nystagmus was recorded using electronystagmography (ENG). Results: Head control and independent walking were delayed in 28 of 97 children with severe hearing loss. Reduced response to the rotational chair test was observed in 16 of 97 children (16.5%), with 11 of these children having inner ear anomalies and reduced vestibular function. Of the 10 children who were followed up by the rotational chair test, 2 children with idiopathic congenital hearing loss without inner ear anomalies (100%) and 6 of 8 children with bilateral inner ear anomalies (75%) showed more obvious nystagmus during rotation compared with the initial examination.
Keywords: Inner ear malformation, rotational chair test
Introduction The developmental neurology of balance impairment in infants and children began from the observation of postural reflex of infants and children. AndrésThomas reported that the presence or absence of labyrinthine righting reflex is important in diagnosing pediatric neurological diseases, and he clarified the characteristics of posture changes and development of the newborn in the mid-20th century. Rapin noticed that a delay in motor development in infancy was often reported in students at the school for hearing impaired children and reported this in a retrospective study in 1974 [1]. Kaga et al. in 1981 examined the vestibulo-ocular reflex (VOR) quantitatively in children with severe hearing loss using a rotational chair and demonstrated that head control and independent walking are delayed when the VOR is lacking [2]. Currently, inner ear morphology can be
observed in detail due to the development of high-resolution CT, and inner ear malformations and narrowing of the internal auditory canal can be revealed. However, there have been no reports that follow up on changes of the VOR due to development. Therefore, we evaluated the vestibular function of children with bilateral severe hearing loss using a rotational chair test. In addition, we performed a follow-up study on the relationship between vestibular function and motor development for which head control and independent walking were used as indicators of motor development. Material and methods Patients A total of 97 children under 4 years old with a hearing threshold for both ears greater than 80 dB and who
Correspondence: Takeshi Masuda, Otolaryngology-Head and Neck Surgery, Nihon University School of Medicine, Tokyo, Japan. E-mail: [email protected]
(Received 9 December 2013; accepted 24 January 2014) ISSN 0001-6489 print/ISSN 1651-2251 online 2014 Informa Healthcare DOI: 10.3109/00016489.2014.890290
Acta Otolaryngol Downloaded from informahealthcare.com by University of Laval on 07/05/14 For personal use only.
Acquisition of vestibular function in children visited the Tokyo Medical Center Hospital for infants and children with hearing loss and language disorders during the 5 years between June 2008 and October 2013 were studied. None of the children had had cochlear implant surgery before the initial examination. Their ages ranged from 3 months to 37 months, with an average age of 23.1 months and a median age of 22.5 months. Assessment of hearing was determined comprehensively using the auditory steady state response (ASSR), auditory brainstem response (ABR) test, and conditioned orientation reflex (COR) to measure the hearing threshold. We use not only ABR but ASSR and COR when a child has the possibility of low tone hearing. Genetic testing related to hearing was conducted in a small number of the patients whose parents requested it and the results of the genetic testing were not included in the evaluation. Inner ear malformations were classified according to the classification by Sennaroglu and Saatci [3]. Head control (the state in which a motion of the head is controllable by itself) and independent walking (the state in which there is no support and the child can walk by him or herself) were used as indicators of motor development. Based on the results of an infant and children physical development survey report in 2010 conducted by the Ministry of Health, Labour and Welfare of Japan, a delay in motor development was determined when head control was later than 5 months and independent walking was later than 14 months, which are the 97th percentile values. Head control and independent walking were checked using the mother-and-baby notebook for medical and welfare records, the notebook handed out by local public organizations in Japan. We followed up the children that were under 6 months old for 1 year or more. In cases of premature birth, the children were evaluated using a corrected age.
673
the horizontal direction. An electrical calibration with 100 mV was used for calibration of eye movement. The number of beats of nystagmus during rotation and duration of time for nystagmus were measured and the average values of the left and right rotations were obtained. When both were less than 50% of the age control data of Kaga et al. [2], the vestibular function was determined to be reduced. Results The causes of hearing loss in the 97 children with bilateral severe hearing loss were idiopathic congenital hearing loss in 66 children, bilateral inner ear malformation in 12 children, cytomegalovirus (CMV) infection in 5 children, auditory neuropathy in 4 children, symptomatic hearing impairment in 3 children, meningitis in 3 children, large vestibular aqueduct syndrome in 2 children, deaf and blind in 1 child, and hyperbilirubinemia in 1 child (Table I). Motor development was delayed in 28 of 97 children (28.9%). Of these 28 children, 16 (57.1%) showed a reduced response to the rotational chair test. Of the 28 children who showed a delay in motor development, the causes were inner ear malformation in 12 children, idiopathic congenital hearing loss in 10 children, symptomatic hearing impairment in 2 children, CMV infection in 2 children, deaf and blind in 1 child, and large vestibular aqueduct syndrome in 1 child. The response to the rotational chair test was reduced in 16 of 97 children (16.5%). All of these 16 children showed delayed motor development. Of the 16 children who showed reduced response to the rotational chair test, the causes were inner ear malformation in 11 children, idiopathic congenital hearing loss in 4 children, and deaf and blind in 1 child (Figure 1). The follow-up examination performed in two of four children with idiopathic congenital hearing loss
Rotational chair test Table I. Causes of hearing loss and average ages of the children.
Earth-vertical axis rotation (EVAR) was used for the rotational chair test. A damped-rotational chair test similar to the protocol of Kaga et al. [2] was performed using a computer-controlled rotational chair (type S-II; Nagashima Co. Ltd, Tokyo, Japan). For the safety of the children, a parent sat on the rotational chair first and then held the child on their lap during the rotational chair test. The test was performed in the dark to reduce the influence of the visual suppression and the velocity was decelerated by 4 /s from the initial velocity of 160 /s. Right rotation was performed first, followed by left rotation after a 5 min interval. Nystagmus was recorded by electronystagmography (ENG). The electrodes were placed near the lateral canthus of both eyes to record the eye movement in
No. of patients
Average age
Idiopathic congenital hearing loss
66
2 years 0 months
Bilateral inner ear malformation
12
1 year 10 months
Cytomegalovirus infection
5
2 years 6 months
Auditory neuropathy
4
1 year 1 month
Symptomatic hearing impairment
3
1 year 5 months
Meningitis
3
1 year 4 months
Large vestibular aqueduct syndrome
2
1 year 8 months
Hyperbilirubinemia
1
2 years 1 month
1
2 years 7 months
97
1 year 11 months
Cause of hearing impairment
Deaf and blind Total
674
T. Masuda & K. Kaga Per-rotatory nystagmus
Motor development Normal: 69
Normal response: 69
97 patients
Normal response: 12 Delay: 28
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Bilateral inner ear malformation: 12 Idiopathic congenital hearing loss: 10 Symptomatic hearing impairment: 2 Cytomegalovirus infection: 2 Deaf and blind: 1 Large vestibular aqueduct: 1
Poor response: 16 Bilateral inner ear malformation: 11 Idiopathic congenital hearing loss: 4 Deaf and blind: 1
Figure 1. Results of motor development and nystagmus during rotation. Among 97 children, 16 of 28 who showed a delay in motor development also showed a reduced response to the rotation test. Motor development was normal in 69 children, and all showed a normal response to the rotation test.
whose vestibular function was reduced at the initial examination showed that distinct nystagmus began to appear in all children (Table II). The follow-up examination of the eight children with inner ear malformation showed that distinct nystagmus began to appear compared with the initial examination in six children (Table III). The number of beats of nystagmus during rotation and the duration of time for nystagmus were plotted through the time course for 10 children who were followed up, as described above, and compared with the control data of Kaga et al. [2]. The number of beats of nystagmus increased with age in 8 of the 10 children, but not in the other 2 children (nos 4 and 7). Despite the fact that children nos 3 and 8 showed no response in the initial examination, they began to show a better response than the control data (Figure 2). The duration of time for nystagmus was increased with age in eight children, but not in nos 4 and 7. Seven children (nos 1, 3, 5, 6, 8, 9, and 10) developed a good response that exceeded the control data (Figure 3). Discussion Motor development in children with congenital severe hearing loss is often delayed. A reason for delayed
head control and independent walking may be the loss of muscle from the vestibule and, thus, sufficient tension cannot be maintained [4]. In children with severe hearing loss, not only hearing, but also the vestibular nerve and vestibular sensory cells may have abnormalities that cause a delay in motor development [5]. This study also showed that motor development, such as head control and independent walking, was delayed in 28 of 97 children with severe hearing loss. Some reports have evaluated vestibular function in children [6–8], but it is difficult to perform vestibular function testing in infants. However, it is possible to evaluate vestibular function quantitatively even in infants from whom cooperation is not obtained, by using a damped-rotational chair test. Eviatar et al. [9] conducted a caloric test and rotation test in 276 infants aged from 1 day to 1 year old and divided into four groups by every 3 months after birth. Nystagmus was more difficult to elicit in the younger age children in the caloric test, whereas it appeared regardless of age in the rotation test. As evidenced by a canal plugging experiment in monkeys, the rotation test is one of the most stimulating tests among the vestibular function tests because it applies stimulus to the semicircular canals and otolith organs in both ears [10]. Therefore, it can detect the response even when the VOR is very weak.
Table II. Follow-up results of the damped-rotational chair test in children with normal inner ear morphology. Child no. 1
Age
Disease
1 year 10 months
Idiopathic congenital hearing loss
3 years 10 months 2
1 year 10 months 3 years 1 month
Idiopathic congenital hearing loss
Time duration (s)
No. of beats
Head control
Independent walking
0
0
5 months
1 year 10 months
32.5
16
2 years 7 months, right
12 months
1 year 10 months
–
2.5 13
2.5
CI
13
In two children with idiopathic hearing loss without morphological anomalies in the inner ear, a distinct vestibulo-ocular reflex (VOR) compared with the initial examination appeared. CI, age when cochlear implant surgery was performed.
Acquisition of vestibular function in children
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Table III. Follow-up results of the damped-rotational chair test in children with inner ear malformation. No. 3
Age 6 months
Type of cochlear anomaly Bilateral IP-II
Type of vestibular anomaly
Time duration (s)
No. of beats
Head control
0
0
6 months
37
40.5
1 year 4 months
2 years 0 months, left
10 months
1 year 10 months
2 years 10 months, left
6 months
1 year 6 months
1 year, 10 months, right
6 months
1 year 1 month
2 years 1 month, left
8 months
1 year 10 months
3 years 10 months, left
6 months
1 year 10 months
2 years 4 months, right
6 months
1 year 6 months
2 years 8 months, right
6 months
1 year 4 months
3 years 4 months, right
Bilateral normal
1 year 10 months 4
6 months
Bilateral IP-II
Bilateral vestibular hypoplasia
0
0
0
0
1 year 11 months
0
0
3 years 2 months
2
2
1 year 4 months
5
6 months
6
9 months 1 year 2 months
Bilateral common cavity
Bilateral common cavity
Left IP-II, right IP-I
Bilateral normal
7
1 year 9 months 3 years 2 months
0
0
31.5
28.5
0
0
9.5
2 years 0 months
28 Left IP-I, right Michel
Left normal, right Michel
12.5
2 years 3 months
Left IP-I, right cochlear hypoplasia
Left normal, right vestibular hypoplasia
3 years 7 months 9
2 years 6 months 3 years 5 months
Bilateral common cavity
Bilateral common cavity
Bilateral IP-I
Bilateral normal
4 years 9 months 10
3 years 3 months
8
7.5
7
0
0
29.5
34
3.5
3.5
0
0
39
28
37
CI
21
3.5
6
5 years 7 months
11
2.5
3 years 5 months 8
3.5 22
In six of eight children (75%) with inner ear malformation, a distinct vestibulo-ocular reflex (VOR) appeared compared with the initial examination. CI, age when cochlear implant surgery was performed; IP-I, incomplete partition type I; IP-II, incomplete partition type II [3].
Number of beats 45 No.3 40 No.8
35 Number of times
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4 years 7 months
Independent walking
Control
30 No.5 25
No.9 No.10
No.6
20
No.1 No.2
15 10
No.7
5 No.4
0 0
6m
1y 1y6m 2y 2y6m 3y 3y6m 4y 4y6m 5y 5y6m 6y (age)
Figure 2. The time course and the number of beats of nystagmus during rotation of all 10 children who had a follow-up examination. Except for nos 4 and 7, eight children showed an increase with growth in the number of beats of nystagmus during rotation. In particular, nos 3 and 8 began to show a better response than the control data despite no reaction in the initial examination. The dashed line indicates control data from Kaga et al. [2].
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T. Masuda & K. Kaga Duration of time for nystagmus 45 No.9
40
No.10
No.3
35
No.1 No.5
(sec)
30
No.6
No.8
25 Control
20 15
No.7
No.2
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10 5 No.4 0 0
6m
1y 1y6m 2y 2y6m 3y 3y6m 4y 4y6m 5y 5y6m 6y (age)
Figure 3. The time course and duration of time for nystagmus of all 10 children who had a follow-up examination. Similar to Figure 2, 8 of the 10 children (except nos 4 and 7) showed an increase with growth in the duration of time for nystagmus. In particular, seven children (nos 1, 3, 5, 6, 8, 9, and 10) showed a good response that exceeded the control data. The dashed line indicates control data from Kaga et al. [2].
Since 2008 in our facility, the damped-rotational chair test has been performed and vestibular function, along with motor development, has been evaluated before cochlear implant surgery. In the results, 16 of 97 children showed reduced response to the dampedrotational chair test and all of these 16 children showed delayed motor development. In particular, 11 of 12 children with bilateral inner ear malformation showed delayed motor development (Figure 1). The follow-up examination was carried out for 10 of 16 children with reduced response to the initial rotational chair test. Of these 10 children, idiopathic congenital hearing loss was observed in 2 children and inner ear malformation was observed in 8 children. As a result, both the two children with idiopathic congenital hearing loss (100%) and six of eight children with inner ear malformation (75%) began to show a distinct VOR compared with the initial examination. The result of the rotational chair test was normal in 12 of 28 children who had delayed motor development. A rotational chair test stimulates both the ears. Therefore, the stimulus is stronger than a caloric test 1.Vestibular nerve
or VEMP, and cannot detect a laterality and slight reduction of VOR. When using a caloric test or VEMP in these 12 children, abnormalities may have been detected. Jin et al. [11] performed the VEMP test in seven children with inner ear malformation after cochlear implant surgery and evaluated the presence or absence of the response. All children showed VEMP responses when the power of the cochlear implant was turned on. This result suggests that the vestibular nerve is present even if there is an inner ear malformation. The reason why the VOR did not appear in the initial examination, but began to appear in the followup in this study, was considered separately in the presence or absence of inner ear malformation. In order for the VOR to appear in the rotational chair test when there are no morphological anomalies in the inner ear, the cupula must function as a sensor and the vestibular nerve must transmit signals into the brainstem. According to current knowledge of embryology, the membranous labyrinth is completed in viviparous 9 months. However, the vestibular sensory
2.Sensory neuron (Cupula)
3.Vestibular nerve & Cupula
Vestibular nerve
Cochlear nerve
Sensory neuron (Cupula)
Figure 4. Acquisition of the vestibulo-ocular reflex (VOR) in children with normal inner ear morphology. (1) Development of the vestibular nerve. (2) Maturation of balance sensory cells (cupula). (3) Both (1) and (2).
Acquisition of vestibular function in children 1.Vestibular nerve
2.Sensory neuron (Macula) Sensory neuron (Macula) Vestibular nerve
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3.Vestibular nerve & sensory neuron
Cochlear nerve
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Figure 5. Acquisition of the vestibulo-ocular reflex (VOR) in children with inner ear malformation. (1) Development of vestibular nerve. (2) Maturation of the macula (vestibular sensory cells). (3) Both (1) and (2).
neurons are completed at the 23 weeks stage. Furthermore, the vestibular nerve is completed at 5 months, although the form of the membranous labyrinth is in the same state as at 6 weeks of viviparous time in common cavity malformation, after which myelinization of the vestibular nerve and maturation of the sensory cells take place [12,13]. Figures 4 and 5 are drawn from current embryological knowledge. The appearance of the VOR with age in children with no inner ear anomalies may be due to maturation of the vestibular nerve, maturation of balance sensory cells, or both (Figure 4). In regard to cases with inner ear malformations, common cavity malformations were examined as an example. In EVAR, which was performed in this study, the cupula of the lateral semicircular canals was stimulated primarily in cases with normal inner ear morphology. However, for children with an inner ear malformation, since the fixed axis does not exist in the vestibular organs, the otolith organs are stimulated similar to when OVAR (off-vertical axis rotation) stimulus is used. The appearance of the VOR with age in children with inner ear malformation may be due to maturation of the vestibular nerve, maturation of the macula (vestibular sensory cells), or both (Figure 5). Children with inner ear malformation show a delay in motor development in their infancy, but acquire vestibular compensation from the central nervous system (CNS) or muscle tone due to the reflex from the vestibular labyrinth and growth. By junior high or high school stage, the children can perform most exercises without problems [4]. The present study reconfirmed that head control and independent walking are delayed if the acquisition of the VOR is insufficient. However, the VOR may be acquired with growth even if it is reduced during early childhood. It is necessary to accurately evaluate vestibular function in children to determine the proper rehabilitation strategy [14]. This study does not clarify completely the relationship between the vestibular function and motor development in children with severe hearing loss. Further studies, including analysis of genetic abnormalities and mental retardation, as well as multiple disabilities in children are required.
Conclusions (1) Twenty-eight of 97 children with bilateral severe hearing loss showed a delay in head control or independent walking. (2) The damped-rotational chair test was performed in 97 children younger than 4 years old with severe hearing loss. Sixteen children (17%) showed no response or severely reduced response. Of those, 11 of 12 children (91.7%) with inner ear malformation showed reduced vestibular function. (3) Of the 10 children who were followed up with the rotational chair test, the VOR began to appear with growth in the 2 children without inner ear malformation (100%) and in 6 of 8 children with bilateral inner ear malformation (75%). (4) These results suggest that vestibular function may be acquired due to the maturation of vestibular sensory cells and vestibular nerve in the inner ear along with growth in children with severe hearing loss and reduced vestibular function.
Acknowledgment The authors thank Mrs Yakushimaru for her clinical examination work. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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