International Journal of Pediatric Otorhinolatyngology, 23 (19Y2) 261-268 0 1992 Elsevier Science Publishers B.V. All rights reserved 01655876/92/$05.00
PEDOT
‘61
00769
Delayed motor function and results of vestibular function tests in children with inner ear anomalies Toshihiro Tsuzuku and Kimitaka Kaga Department of Otolaryngology, Teikyo lJnil,ersity School of Medicine, Tokyo, Japan (Received 5 December 1990) (Revised version received 23 April 1991) (Accepted 27 April 1991)
Key words: Inner
ear anomaly;
Motor
function;
Caloric
test, Damped
rotation:
Barany
rotation
Abstract
The relation between the results of vestibular function tests and gross motor development was examined in 4 children with inner ear anomalies. CT scans demonstrated the absence of lateral semicircular canals in both ears in all 4 cases. None responded to caloric stimulation using 40 ml of icewater. In contrast, the damped rotation test elicited per-rotatory nystagmus in all cases. Per-rotatory nystagmus was provoked in only two cases by the Barany rotation test. Development of gross motor function, especially independent walking, was more delayed in the two children in whom the Barany rotation test failed to elicit per-rotatory nystagmus.
Introduction
Development of motor function has been shown to be retarded in certain children with congenital deafness [2-4, 6-81, particularly in patients with an inner ear anomalies [7]. The relation between the results of vestibular function tests and the development of motor function in 4 children with inner ear anomalies is examined in this study. Correspondence: T. Tsuzuku, Department of Otolaryngology. 2-l 1-l Kaga, Itabashi-ku, 173 Tokyo, Japan.
Teikyo
University
School
of Medicine.
262
History of the 4 patients Case 1
The patient was a lo-year-old boy who complained of profound bilateral hearing loss. He was the product of an uncomplicated pregnancy, labor and delivery. There was no family history of deafness. Congenital obstruction of the choanae and ventricular septal defect were detected at birth. The patient was fitted with a hearing aid soon after bilateral hearing loss was documented at the age of two years 6 months. His acquisition of gross motor function, such as head control, sitting, crawling and walking, was markedly delayed (see Fig. 4). The patient was evaluated in our clinic at the age of 6 years. Clinical examinations. The results of pure-tone audiometry showed bilateral profound sensorineural hearing loss. Case 2
The patient was a lo-year-old boy who suffered from hearing loss. There was no history of complications of pregnancy, labor or delivery or of deafness in his family. At the age of one-and-a-half years, when bilateral hearing loss was suspected, he was fitted with a hearing aid and given special education for deaf children. The patient became able to speak words by age 3. His acquisition of gross motor function was delayed, and he was referred to our speech and hearing clinic for an objective hearing test when he was 3 years old. Clinical examinations. Profound bilateral sensorineural hearing loss was revealed by pure tone audiometry. Case 3
The patient was a 3-year-old boy suspected of bilateral hearing loss. There was no family history of deafness. Delivery was normal, but the patient was found to have congenital obstruction of the oesophagus and patent ductus arteriosus. At the age of 6 months, he was referred to our clinic by the cardiovascular department because of poor response to sound. Although his gross motor development was retarded, the patient walked earlier than patients 1 or 2. Clinical examinations. Auditory brainstem response revealed no response at 110 dB nHL. Case 4
The patient was a 3-year-old girl who showed poor response to sound. Pregnancy and delivery were normal. No family history of deafness was noted. At the age of 6 months, the patient’s mother noticed that she did not respond to sounds and brought her to our clinic. Clinical examinations. No response was confirmed at 110 dB nHL in auditory brainstem response testing. A summary of hearing thresholds and other anomalies is shown in Table I.
TABLE
J
A summary
of heuring thresholds und other anomulies Hearing thresholds
Other anomulirs
caseI
100 dB *
Case 1 Case 3
100 dB * llOdBnHL**
Case 4
1 IO dB nHL * *
Congenital V.S.D. None Congcnltal P.D.A. None
* Pure ton2 ** ABR (0.1
obstruction
of choanae
obstruction
of oesophagus
500 HZ + 1 kHz + 2 kHz __.~______ ms 4kHz c&k).
Findings CT scan CT scans of the temporal bones revealed several different types of anomalies in the cochlear and vestibular structures. Fig. 1 shows the CT scan of patient 1. Fig. 2 shows schematic drawings of our cases based on the temporal bone CT scan to have no studies of Valvassori et al. [8] and Akai et al. [l]. Patient 1 appeared
Lt
Rt
Fig. 1. Serial CT scan sections of the temporal bone in case 1. There appeared to be no semicircular canal in either ear. 1, basal turn of the cochlea. 2, basal and middle turns of the cochlea. Note that no apical turns are identified. 3, internal auditory meatus. 4, vestibule, part of the utricle and saccule. Note that no lateral semicircular canal is seen. 5, no posterior or anterior semicircular canals are observed.
Fig. 2. Schematic drawings of inner ear anomalies on both sides in our 4 cases. The white areas represent congenitally absent portions of the inner ears and the black areas represent the portions suspected to be present.
semicircular canals in either ear; the other 3 children had no lateral or posterior semicircular canals. Clinical examination of vestibular function
In order to evaluate vestibular function in these children, caloric tests and two different types of rotation tests, the damped rotation test and the Barany rotation test, were performed. Caloric tests Procedure and Results.
Caloric tests were conducted in the optimal supine head position with Frenzel’s spectacles, using 40 ml of icewater. As predicted from the CT findings, there was no nystagmic response to this strong caloric stimulation of either ear in any of the patients. Rotation tests Two different kinds of rotation test were performed. In the case of Procedure. the damped rotation test, we used the spring-driven damped-rotation chair devel-
oped at our clinic for rotation nystagmus. Rotation of the chair was adjusted by means of a counterweight to deliver a maximum acceleration of approximately 300 degrees/s2 and a speed of approximately 200 degrees/s, and so that it would to stop after 6 rotations (about 20 s). In the case of the Ba’r&y rotation test, chair
765
Damped rotation test IIc-----lll
-
V A
V
-x--+_J
Fig. 3 Electronystagmographic recordings of the B&&y rotation and damped rotation test in all 4 cases. R stands for rotation to the right and L for rotation to the left. A or T indicates onset of rotatory stimulation, and A or v indicates end of rotatory stimulation.
rotation was adjusted by counterweight to deliver a maximum acceleration of approximately 40 degrees/s’ and to stop after 10 rotations with in 20 s. In children, the evaluation of post-rotatory nystagmus was difficult, therefore, we appraised per-rotatory nystagmus. Results (Fig. 3). Although the damped rotation test elicited per-rotatory nystagmus in all cases, the duration and total number of nystagmic beats in these 4
266
Head control Sitting Crawling Walking I
Fig. 4. Correlation
Ocontrols between
v patient
$1
n 52
0 $3
Aa
age and motor function
development.
children were less than in normal children of the same age [3]. In contrast, the results of the Barany rotation test showed induction of per-rotatory nystagmus in case 3 and 4, but the beats and amplitude were also less than in normal children of the same age. Development of gross motor function
The ages at which the patients achieved a particular motor function, such as independent walking, are shown in Fig. 4. All 4 children reached these milestones later than normal children. The age at which patients 1 and 2 achieved independent walking was later than in cases 3 and 4.
Discussion
The delayed development of motor function in cases of inner ear anomalies may be the result of insufficient vestibular input, including insufficient sense of equilibrium and labyrinthine tonus from abnormal semicircular canals. Even in such cases, children do learn to walk albeit late. Development of this motor skill presumably depends on compensatory input from other sensory systems such as projection and vision and/or the maturation of motor systems in the cerebellum, basal ganglia and motor cortex. Patient 3, who had rather asymmetric damage, achieved head control later, and independent walking earlier, than the other children. His oesophagus was reconstructed after birth, but his general development was retarded until cardiovascular surgery was performed. This retardation may have affected his head control. The recovery of development after cardiovascular surgery and well-preserved vestibular function as a result of having two semicircular canals in his right ear, may have played a role in his early achievement of independent walking. As revealed by CT scan, the bony structures of the inner ears of these cases were not fully developed. This abnormality must arise during early embryogenesis,
267
because formation of the bony structures of the vestibule is completed during the first 10 weeks of gestation. In humans, the membranous labyrinth is fully developed in the vestibule by about the 12th week and in the cochlea by about the 28th week of gestation. Based on our own findings, it is difficult to discuss the membranous labyrinth. It might have been abnormal, because in all of our cases the bony structures of the inner ear appeared at about 10 weeks of gestation, and as a result the features of our cases might be classified as being of the Mondini type. Although none of our patients had lateral semicircular canals, they responded positively but poorly in the damped rotation test, compared with normal children of the same age. Their responses could not have been artifacts because their heads were fixed in a head-support with their noses angled downward at approximately 30 o during testing. In this position the horizontal canals were almost parallel to the horizontal plane of the earth’s surface. The chamber was entirely dark. so there was no contamination by visual input. In recent study in the rat, Kubo et al. reported that vertical axis rotation with the head tilted produced simultaneous stimulation of not only the horizontal canal but the other semicircular canals and otoliths [S]. The otolithic function on these patients is unknown, since clinical evaluation of otolithic function is very complicated, and our patients were too young to test. The positive response to the rotatory test in our patients may be attributable to the remaining vestibular functions. When the Barhny rotation test and ice water irrigation caloric test were compared, although the former was capable of strongly stimulating the vestibule and per-rotatory nystagmus was provoked, no caloric nystagmus was elicited in the caloric test. When the Barany rotation test and damped rotation test were compared in cases of inner ear anomalies, on the other hand, while the former may have provided weaker stimulation to the vestibule and no per-rotatory nystagmus was provoked in cases of severely impaired vestibular function, per-rotatory nystagmus was provoked by the damped rotation test in all of the patients. In the two cases of inner ear anomalies which responded to the Barany rotation test, remaining vestibular function must have acted as a compensatory system for motor development. This study suggests that evaluation of motor function development in children with inner ear anomalies is better correlated with the results of the Barany rotation test than those of the caloric or damped rotation test.
References 1 Akai. S.. Hashimoto, H., Kanoh, Y., Yamada, 0. tomography: a new projection to the temporal bone. 2 Buruk A., Ueber die Beziehungen der Taubstummheit Arch. Ge.7. Physiol., 59 (1895) 16-42. 3 Kaga, K., Suzuki. J., Marsh, R.R., and Tanaka, Y., motor development of infants. Ann. N.K Acud. Sci.,
and Suzuki, _I., Semi-axial view by computed Teikyo Med. J., 6 (1983) 305-310 (in Japanese). zum sogenannten statischen Sinn. Pflue,q~3 influence of labyrinthine 374 (lY81) 412-420.
hypoactivity
on gross
268 4 Kreidel, A., Beitrage zur Physiologie des Ohrlabyrinths auf Grund von Versuchen an Taubstummen, Pflueger’s Arch. ges. Physiol., 51 (1892) 119-150. 5 Kubo, T., Matsumaga, T., and Matano, S., Convergence of ampullar and macular inputs on vestibular nuclei unit of the rat, Acta Otohryngol., 84 (1977) 166-177. 6 Precechtel, A., Contribution a l’etude de la fonction statique dans la periode foetal et dans la premiere periode de la vie extrauterine; syndrome typique du defaut congenital infantile otolithique, Acta Otolaryngol., 7 (1927) 206-226. 7 Suzuki, J., Kaga, K. and Yabuki, K., Observations of vestibular functions in 4 patients with inner ear anomaly. In J.C. Hwang, N.G. Dauton and V.I. Wilson (Eds.), Basic and Applied Aspects of Vestibuhr Function, Hong Kong University Press, Hong Kong, 1988, pp. 153-163.
8 Valvassori, G.E. , Naunton, R.F. and Lindsay, J.R., Inner ear anomalies: clinical and histopathological considerations, Ann. Otol. Rhinol. Laryngol., 78 (1969) 929-938.
PEDOT
‘61
00769
Delayed motor function and results of vestibular function tests in children with inner ear anomalies Toshihiro Tsuzuku and Kimitaka Kaga Department of Otolaryngology, Teikyo lJnil,ersity School of Medicine, Tokyo, Japan (Received 5 December 1990) (Revised version received 23 April 1991) (Accepted 27 April 1991)
Key words: Inner
ear anomaly;
Motor
function;
Caloric
test, Damped
rotation:
Barany
rotation
Abstract
The relation between the results of vestibular function tests and gross motor development was examined in 4 children with inner ear anomalies. CT scans demonstrated the absence of lateral semicircular canals in both ears in all 4 cases. None responded to caloric stimulation using 40 ml of icewater. In contrast, the damped rotation test elicited per-rotatory nystagmus in all cases. Per-rotatory nystagmus was provoked in only two cases by the Barany rotation test. Development of gross motor function, especially independent walking, was more delayed in the two children in whom the Barany rotation test failed to elicit per-rotatory nystagmus.
Introduction
Development of motor function has been shown to be retarded in certain children with congenital deafness [2-4, 6-81, particularly in patients with an inner ear anomalies [7]. The relation between the results of vestibular function tests and the development of motor function in 4 children with inner ear anomalies is examined in this study. Correspondence: T. Tsuzuku, Department of Otolaryngology. 2-l 1-l Kaga, Itabashi-ku, 173 Tokyo, Japan.
Teikyo
University
School
of Medicine.
262
History of the 4 patients Case 1
The patient was a lo-year-old boy who complained of profound bilateral hearing loss. He was the product of an uncomplicated pregnancy, labor and delivery. There was no family history of deafness. Congenital obstruction of the choanae and ventricular septal defect were detected at birth. The patient was fitted with a hearing aid soon after bilateral hearing loss was documented at the age of two years 6 months. His acquisition of gross motor function, such as head control, sitting, crawling and walking, was markedly delayed (see Fig. 4). The patient was evaluated in our clinic at the age of 6 years. Clinical examinations. The results of pure-tone audiometry showed bilateral profound sensorineural hearing loss. Case 2
The patient was a lo-year-old boy who suffered from hearing loss. There was no history of complications of pregnancy, labor or delivery or of deafness in his family. At the age of one-and-a-half years, when bilateral hearing loss was suspected, he was fitted with a hearing aid and given special education for deaf children. The patient became able to speak words by age 3. His acquisition of gross motor function was delayed, and he was referred to our speech and hearing clinic for an objective hearing test when he was 3 years old. Clinical examinations. Profound bilateral sensorineural hearing loss was revealed by pure tone audiometry. Case 3
The patient was a 3-year-old boy suspected of bilateral hearing loss. There was no family history of deafness. Delivery was normal, but the patient was found to have congenital obstruction of the oesophagus and patent ductus arteriosus. At the age of 6 months, he was referred to our clinic by the cardiovascular department because of poor response to sound. Although his gross motor development was retarded, the patient walked earlier than patients 1 or 2. Clinical examinations. Auditory brainstem response revealed no response at 110 dB nHL. Case 4
The patient was a 3-year-old girl who showed poor response to sound. Pregnancy and delivery were normal. No family history of deafness was noted. At the age of 6 months, the patient’s mother noticed that she did not respond to sounds and brought her to our clinic. Clinical examinations. No response was confirmed at 110 dB nHL in auditory brainstem response testing. A summary of hearing thresholds and other anomalies is shown in Table I.
TABLE
J
A summary
of heuring thresholds und other anomulies Hearing thresholds
Other anomulirs
caseI
100 dB *
Case 1 Case 3
100 dB * llOdBnHL**
Case 4
1 IO dB nHL * *
Congenital V.S.D. None Congcnltal P.D.A. None
* Pure ton2 ** ABR (0.1
obstruction
of choanae
obstruction
of oesophagus
500 HZ + 1 kHz + 2 kHz __.~______ ms 4kHz c&k).
Findings CT scan CT scans of the temporal bones revealed several different types of anomalies in the cochlear and vestibular structures. Fig. 1 shows the CT scan of patient 1. Fig. 2 shows schematic drawings of our cases based on the temporal bone CT scan to have no studies of Valvassori et al. [8] and Akai et al. [l]. Patient 1 appeared
Lt
Rt
Fig. 1. Serial CT scan sections of the temporal bone in case 1. There appeared to be no semicircular canal in either ear. 1, basal turn of the cochlea. 2, basal and middle turns of the cochlea. Note that no apical turns are identified. 3, internal auditory meatus. 4, vestibule, part of the utricle and saccule. Note that no lateral semicircular canal is seen. 5, no posterior or anterior semicircular canals are observed.
Fig. 2. Schematic drawings of inner ear anomalies on both sides in our 4 cases. The white areas represent congenitally absent portions of the inner ears and the black areas represent the portions suspected to be present.
semicircular canals in either ear; the other 3 children had no lateral or posterior semicircular canals. Clinical examination of vestibular function
In order to evaluate vestibular function in these children, caloric tests and two different types of rotation tests, the damped rotation test and the Barany rotation test, were performed. Caloric tests Procedure and Results.
Caloric tests were conducted in the optimal supine head position with Frenzel’s spectacles, using 40 ml of icewater. As predicted from the CT findings, there was no nystagmic response to this strong caloric stimulation of either ear in any of the patients. Rotation tests Two different kinds of rotation test were performed. In the case of Procedure. the damped rotation test, we used the spring-driven damped-rotation chair devel-
oped at our clinic for rotation nystagmus. Rotation of the chair was adjusted by means of a counterweight to deliver a maximum acceleration of approximately 300 degrees/s2 and a speed of approximately 200 degrees/s, and so that it would to stop after 6 rotations (about 20 s). In the case of the Ba’r&y rotation test, chair
765
Damped rotation test IIc-----lll
-
V A
V
-x--+_J
Fig. 3 Electronystagmographic recordings of the B&&y rotation and damped rotation test in all 4 cases. R stands for rotation to the right and L for rotation to the left. A or T indicates onset of rotatory stimulation, and A or v indicates end of rotatory stimulation.
rotation was adjusted by counterweight to deliver a maximum acceleration of approximately 40 degrees/s’ and to stop after 10 rotations with in 20 s. In children, the evaluation of post-rotatory nystagmus was difficult, therefore, we appraised per-rotatory nystagmus. Results (Fig. 3). Although the damped rotation test elicited per-rotatory nystagmus in all cases, the duration and total number of nystagmic beats in these 4
266
Head control Sitting Crawling Walking I
Fig. 4. Correlation
Ocontrols between
v patient
$1
n 52
0 $3
Aa
age and motor function
development.
children were less than in normal children of the same age [3]. In contrast, the results of the Barany rotation test showed induction of per-rotatory nystagmus in case 3 and 4, but the beats and amplitude were also less than in normal children of the same age. Development of gross motor function
The ages at which the patients achieved a particular motor function, such as independent walking, are shown in Fig. 4. All 4 children reached these milestones later than normal children. The age at which patients 1 and 2 achieved independent walking was later than in cases 3 and 4.
Discussion
The delayed development of motor function in cases of inner ear anomalies may be the result of insufficient vestibular input, including insufficient sense of equilibrium and labyrinthine tonus from abnormal semicircular canals. Even in such cases, children do learn to walk albeit late. Development of this motor skill presumably depends on compensatory input from other sensory systems such as projection and vision and/or the maturation of motor systems in the cerebellum, basal ganglia and motor cortex. Patient 3, who had rather asymmetric damage, achieved head control later, and independent walking earlier, than the other children. His oesophagus was reconstructed after birth, but his general development was retarded until cardiovascular surgery was performed. This retardation may have affected his head control. The recovery of development after cardiovascular surgery and well-preserved vestibular function as a result of having two semicircular canals in his right ear, may have played a role in his early achievement of independent walking. As revealed by CT scan, the bony structures of the inner ears of these cases were not fully developed. This abnormality must arise during early embryogenesis,
267
because formation of the bony structures of the vestibule is completed during the first 10 weeks of gestation. In humans, the membranous labyrinth is fully developed in the vestibule by about the 12th week and in the cochlea by about the 28th week of gestation. Based on our own findings, it is difficult to discuss the membranous labyrinth. It might have been abnormal, because in all of our cases the bony structures of the inner ear appeared at about 10 weeks of gestation, and as a result the features of our cases might be classified as being of the Mondini type. Although none of our patients had lateral semicircular canals, they responded positively but poorly in the damped rotation test, compared with normal children of the same age. Their responses could not have been artifacts because their heads were fixed in a head-support with their noses angled downward at approximately 30 o during testing. In this position the horizontal canals were almost parallel to the horizontal plane of the earth’s surface. The chamber was entirely dark. so there was no contamination by visual input. In recent study in the rat, Kubo et al. reported that vertical axis rotation with the head tilted produced simultaneous stimulation of not only the horizontal canal but the other semicircular canals and otoliths [S]. The otolithic function on these patients is unknown, since clinical evaluation of otolithic function is very complicated, and our patients were too young to test. The positive response to the rotatory test in our patients may be attributable to the remaining vestibular functions. When the Barhny rotation test and ice water irrigation caloric test were compared, although the former was capable of strongly stimulating the vestibule and per-rotatory nystagmus was provoked, no caloric nystagmus was elicited in the caloric test. When the Barany rotation test and damped rotation test were compared in cases of inner ear anomalies, on the other hand, while the former may have provided weaker stimulation to the vestibule and no per-rotatory nystagmus was provoked in cases of severely impaired vestibular function, per-rotatory nystagmus was provoked by the damped rotation test in all of the patients. In the two cases of inner ear anomalies which responded to the Barany rotation test, remaining vestibular function must have acted as a compensatory system for motor development. This study suggests that evaluation of motor function development in children with inner ear anomalies is better correlated with the results of the Barany rotation test than those of the caloric or damped rotation test.
References 1 Akai. S.. Hashimoto, H., Kanoh, Y., Yamada, 0. tomography: a new projection to the temporal bone. 2 Buruk A., Ueber die Beziehungen der Taubstummheit Arch. Ge.7. Physiol., 59 (1895) 16-42. 3 Kaga, K., Suzuki. J., Marsh, R.R., and Tanaka, Y., motor development of infants. Ann. N.K Acud. Sci.,
and Suzuki, _I., Semi-axial view by computed Teikyo Med. J., 6 (1983) 305-310 (in Japanese). zum sogenannten statischen Sinn. Pflue,q~3 influence of labyrinthine 374 (lY81) 412-420.
hypoactivity
on gross
268 4 Kreidel, A., Beitrage zur Physiologie des Ohrlabyrinths auf Grund von Versuchen an Taubstummen, Pflueger’s Arch. ges. Physiol., 51 (1892) 119-150. 5 Kubo, T., Matsumaga, T., and Matano, S., Convergence of ampullar and macular inputs on vestibular nuclei unit of the rat, Acta Otohryngol., 84 (1977) 166-177. 6 Precechtel, A., Contribution a l’etude de la fonction statique dans la periode foetal et dans la premiere periode de la vie extrauterine; syndrome typique du defaut congenital infantile otolithique, Acta Otolaryngol., 7 (1927) 206-226. 7 Suzuki, J., Kaga, K. and Yabuki, K., Observations of vestibular functions in 4 patients with inner ear anomaly. In J.C. Hwang, N.G. Dauton and V.I. Wilson (Eds.), Basic and Applied Aspects of Vestibuhr Function, Hong Kong University Press, Hong Kong, 1988, pp. 153-163.
8 Valvassori, G.E. , Naunton, R.F. and Lindsay, J.R., Inner ear anomalies: clinical and histopathological considerations, Ann. Otol. Rhinol. Laryngol., 78 (1969) 929-938.
