Child's Nerv Syst (1991) 7:316-326
mlINS 9 Springer-Verlag 1991
Brain stem auditory-evoked potentials in meningomyelocele * Natural history of Chiari II malformations Toshihiko Nishimura, Koreaki Mori, Yasufumi Uchida, Takayuki Ohira, and Kazumi Tamura Department of Neurosurgery, Kochi Medical School, Kohasu, Okoh-Cho, Nankoku-City, Kochi Pref., 783 Japan Received November 29, 1989/Revised June 26, 1990
Abstract.
Brain stem auditory-evoked potentials ( B A E P s ) were r e c o r d e d in 30 p a t i e n t s w i t h m e n i n g o m y e locele a n d s h u n t e d h y d r o c e p h a l u s r a n g i n g in age f r o m b i r t h to 33 years. T w e n t y - t w o o f t h e m h a d C h i a r i II m a l f o r m a t i o n , o n e o f w h i c h w a s s y m p t o m a t i c . I n 22 cases, i n c l u d i n g 15 w i t h C h i a r i II m a l f o r m a t i o n , B A E P s were r e c o r d e d r e p e a t e d l y after p e r i o d s r a n g i n g f r o m 18 m o n t h s to 7 years. T h e results were as follows: (1) I I I - V interpeak latency (IPL) decreased progressively from p r o l o n g e d to the n o r m a l r a n g e w i t h g r o w t h until 25 y e a r s o f age; (2) I - I I I I P L t e n d e d to p r o l o n g g r a d u a l l y f r o m the n o r m a l range; (3) these findings m a y i n d i c a t e t h a t the n a t u r a l h i s t o r y o f C h i a r i I I m a l f o r m a t i o n is d e l a y e d m a t u r a t i o n o f the b r a i n stem a n d i n t e n s i f i c a t i o n in the e l o n g a t i o n a n d s t r e t c h i n g o f the h i n d b r a i n a n d l o w e r c r a n i a l nerves.
Key words: B r a i n stem a u d i t o r y - e v o k e d p o t e n t i a l s (BAEPs) - Chiari II malformation - Meningomyelocele - Brain-stem function - Chronological changes - Magnetic r e s o n a n c e i m a g i n g
T h e C h i a r i I I m a l f o r m a t i o n [1, 3, 11, 12] is o n e a n o m a l y for w h i c h t h e n a t u r a l h i s t o r y is u n k n o w n . I n r e c e n t years, m a g n e t i c r e s o n a n c e i m a g i n g ( M R I ) h a s m a d e it p o s s i b l e to visualize the a n a t o m y o f the h i n d b r a i n in d e t a i l a n d to d i a g n o s e this m a l f o r m a t i o n w i t h o u t difficulty. Several studies, h o w e v e r , suggest a d i s c r e p a n c y bet w e e n the m o r p h o l o g i c a l a b n o r m a l i t y in the h i n d b r a i n a n d the f u n c t i o n a l d i s o r d e r . T h e k i n d s o f cases t h a t prese n t clinical s y m p t o m s o f h i n d b r a i n a n d l o w e r c r a n i a l nerve i n v o l v e m e n t h a v e n o t y e t b e e n p r o p e r l y discussed, h o w e v e r . H o w the b r a i n stem d y s f u n c t i o n c h a n g e s d u r ing g r o w t h h a s also n o t been resolved.
* Presented at the XVII Annual Meeting of the International Society for Pediatric Neurosurgery, Bombay 1989 Offprint requests to: T. Nishimura
We r e p o r t e d o n the b r a i n stem a u d i t o r y - e v o k e d p o t e n tials ( B A E P s ) in C h i a r i I I m a l f o r m a t i o n in 1988 [13]. I n t h a t p a p e r , the effect o f the shunting o p e r a t i o n o n the wave forms a n d the age-wave relationship were discussed. Since then, f o l l o w - u p studies have b e e n d o n e a n d c h r o n o l o g i c a l c h a n g e s o n B A E P in cases w i t h m e n i n g o m y e l o c e l e h a v e been investigated. H e r e we r e p o r t the n e w facts we f o u n d . I n this study, B A E P r e c o r d i n g s were i n v e s t i g a t e d to e v a l u a t e the t r a n s i t i o n o f b r a i n stem d y s f u n c t i o n a n d to determine whether certain abnormalities on BAEP are p r e d i c t i v e o f the d e v e l o p m e n t o f h i n d b r a i n s y m p t o m s .
Materials and methods BAEPs were recorded in 30 patients with meningomyelocele between birth and 33 years of age, including 22 cases of Chiari II malformation. In 22 of 30, including 15 cases of Chiari II malformation, BAEPs were recorded repeatedly at intervals ranging from 18 months to 7 years. In cases with hydrocephalus, BAEP recordings were obtained after a shunting operation in order to rule out the effect of hydrocephalus. The signals were recorded through silver electrodes. Pick-up electrodes were placed on the vertex (Cz); reference electrodes were placed on the ear lobe of the stimulated side and the ground electrode on the forehead (Fp). The electrode impedance was kept below 3K[~. Monoaural auditory stimuli, consisting of rarefaction clicks of 125 ms pulses were delivered through a headphone on each side. The stimulus rate was 8/s and its intensity was 85 dB. A minimum of 1024 responses were averaged. At least two trials were evaluated for each ear and responses were superimposed to demonstrate the consistency. The differential input was filtered for a band pass of 50 H z - 3 KHz. Masking was 35 dB. Analysis time was 10 ms. The latencies of the individual waves were measured from the onset of the triggering pulse to the peak of the individual waves. In the present study, each I, III, and V wave was examined because of their constancy. Interpeak latencies (IPL) from I - I I I , III-V, and I - V waves were measured. As control, the data reported by Matsuzawa [9] was used, which was obtained by the same 85 dB stimulation. Evoked responses were considered abnormal if each of the peak or interpeak latencies was prolonged beyond the upper limits of normal (mean__ 2 SD) or if no response was obtained. The morphological aspects were evaluated on CT scans and MRI. CT scans were examined in all cases and MRI in 25 cases. In cases examined by MRI, the degree of descent of both IV ventricle and medulla oblongata was measured on the sagittal image as parameters of morphological abnormality (Fig. 1).
317
In 4 (cases 23, 24, 27 and 30) of the 30 cases, no associated hydrocephalus was seen, nor was Chiari malformation found. The 26 cases with hydrocephalus were treated with a V-P shunt. In 7, ventricular dilation did not improve, in spite of a functional shunt system. BAEP recordings were investigated after the shunting operation in order to rule out the effect of hydrocephalus. In two cases, BAEP was recorded both before and after the shunting operation. BAEP was recorded in all cases between birth and 33 years of age. In 22 cases BAEPs were recorded repeatedly after periods ranging from 18 months to 7 years.
Results
Clinicalfeatures of 30 cases andfollow-up periods of BAEP The clinical features of 30 cases with meningomyelocele are shown in Table 1. Repair of the meningomyelocele was performed at intervals ranging from the day of birth to 3 months. In most cases with open meningomyelocele, repair was performed on the day of birth. In 22 cases the Chiari II malformation was documented. In the other 8 cases, including 2 with lipomeningomyelocele, Chiari II malformation was not a complicating anatomical observation. Only 1 case suffered stridor as a symptom of hindbrain involvement (case 22). Suboccipital decompression was not performed for this patient because her parents rejected the procedure. She was placed on artificial respiration and died at 6 years of age.
BAEP findings (analysis of a total of 63 examinations) A total of 63 examinations were investigated in 30 cases of meningomyelocele. In the age-wave relationships, two tendencies were recognized. In the first place, although the latencies of wave I were almost within normal range or slightly prolonged, those of wave III were more prolonged and those of wave V much more so. Secondly, the degree of prolongation of each wave latency was more remarkable in the younger than the older group if the cut-off point was established at the age of 10 (Fig. 2). Among 22 cases with Chiari II malformation (cases 1-22), BAEPs were recorded repeatedly in 15 cases (cases 1 15). In 9 cases BAEPs were recorded three times (cases 1-9). In the 8 cases without imaging evidence of the Chiari II malformation (cases 23-30), BAEPs were recorded repeatedly in 7 cases (cases 23-29). In 2 cases BAEPs were recorded three times (cases 23 and 24) (Table 1). The results are shown on Tables 2 - 4 and Fig. 3. At the first examination in the 22 cases with Chiari II malformation (cases 1-22), only I - I I I IPL prolongation was recognized in one case (case 8); only I I I - V IPL prolongation was recognized in 12 cases (cases 1, 2, 4 - 6 , 14, 16-18, 20-22); both I - I I I and I I I - V IPL prolongation were recognized in 7 cases (cases 3, 7, 10-13, 19). Disappearance of waves I, III and V was recognized in 1 case
Fig. 1. The level of foramen m a g n u m and medulla oblongata on the sagittal image of MRI. Upper arrow level of the fastigium, lower arrow level of the medulla oblongata, straight line level of the foramen m a g n u m
Latency
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2Y 3Y 4Y 6Y 8Y 9Y llY 12Y 13Y 14Y 15Y 16V 17Y 18Y 21Y 23Y 25Y 27Y 29Y 33Y Age
Fig. 2. Latency of waves I, III and V in a total of 63 examinations in 30 cases of meningomyelocele. 9 Chiari type II malformation ( + ) , o Chiari type II malformation ( - )
Sex
M M F M F F M F F M F M F M F F M M M M F F F M F F F M M M
Case
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC MMC LMMC MMC MMC LMMC
Diagnosis
Lumbosacral Thoracolumbosacral Lumbosacral Thoracolumbosacral Sacral Lumbosacral Lumbar Thoracolumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Thoracolumbosacral Lumbosacral Thoracolumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral Lumbosacral
Level o f s p i n a bi fid a
+ + + + + + + + + + + + + + + + + + + + + + ----
C h i a r i II malformation ----Stridor ----
Clinical symptoms
+ + + + + + + + + + + + + + + + + + + + + + + + -+ + --
Hydrocephalus
8 4 6 9 9 9 10 13 3 27 5 23 8 15 21 13 33 16 8 1 2 2 1 1 1 5 5 8 1 6
(1) days ye a rs years years ye a rs years ye a rs ye a rs days ye a rs ye a rs ye a rs ye a rs ye a rs ye a rs years years ye a rs ye a rs year ye a rs months month day year, 8 m o n t h s ye a rs months ye a rs year months
years y ear s y ear s y ear s y ear s y ear s years years years, 6 m o n t h s y ear s y ear s y ear s y ear s y ear s years
months year years, 9 m o n t h s years years y ear s years
1 8 9 12 13 12 15 16 2 29 7 25 9 19 27
3 1 3 7 2 10 3
(2)
Age at B A E P recording
Table 1. S u m m a r y o f 30 cases wi th m e n i n g o m y e l o c e l e . M M C , M e n i n g o m y e l o c e l e ; L M M C , l i p o m e n i n g o m y e l o c e l e
years, 8 m o n t h s y ear s y ear s y ear s y ear s y ear s y ear s y ear s y ear s
1 year, 7 m o n t h s 2 years, 6 m o n t h s
2 9 11 14 14 13 17 18 4
(3)
+ + + + + + + +
+ + §
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MRI
OO
319 Table 2. Analysis of a total of 63 examinations. Case lists of each type on BAEP findings: I-III, only I - H I IPL is prolonged; III-V, only III-V IPL is prolonged; Mix, both I - I I I and I I I - V IPL are prolonged; Disappear, waves disappear Type
I-III III-V Mix Disappear Normal
Chiari malformation (+)
Chiari malformation ( - )
BAEP (1)
BAEP (2)
BAEP (3)
BAEP (1)
BAEP (2)
BAEP (3)
8 1, 2, 4, 5, 6, 14, 16, 17, 18, 20, 21, 22 3, 7, 10, 11, 12, 13, 19 9 15
1, 8 4, 6, 7
4,8 7
23, 24, 26, 29, 30
23, 29
23
2, 3, 5, 9, 10, 12, 13, 14 11 15
1,2,3,5,6,9
25, 28
24, 27, 28 25" 26
24
27
a Because of deafness due to Kawasaki's disease
Table 3. Analysis of a total of 63 examinations. Frequency of each type on BAEP findings Type
I-III III-V Mix Disappear Normal
Chiari malformation (+)
Chiari malformation ( - )
BAEP (1)
BAEP (2)
BAEP (3)
BAEP (1)
BAEP (2)
BAEP (3)
1/22 (4.6%) 12/22 (54.6%) 7/22 (31.8%) 1/22 (4.6%) 1/22 (4.6%)
2/15 (13.3%) 3/15 (20.0%) 8/15 (53.3%) 1/15 (6.7%) 1/15 (6.7%)
2/9 (37.t%) 1/9 (11.1%) 6/9 (66.7%) 0/9 (0%) 0/9 (0%)
0/8 (0%) 5/8 (62.5%) 2/8 (25.0%) 0/8 (0%) 1/8 (12.5%)
0/7 (0%) 2/7 (28.6%) 3/7 (42.9%) 1/7 (14.3%) a 1/7 (14.3%)
0/2 (0%) 1/2 (50%) 1/2 (50%) 0/2 (0%) 0/2 (0%)
a Because of deafness due to Kawasaki's disease
Table 4. Frequency of abnormality on I - I I I IPL and I I I - V IPL. IPL, Interpeak latency Type
Chiari malformation (+)
Chiari malformation ( - )
BAEP (1)
BAEP (2)
BAEP (3)
BAEP (1)
BAEP (2)
BAEP (3)
9/22 (40.9%) 8/22 (36.6%) 1/22 (4.6%) 13/22 (59.1%)
11/15 (73.3%) 10/15 (66.7%) 1/15 (6.6%) 4/15 (26.7%)
8/9 (88.9%) 8/9 (88.9%) 0/9 (0%) 1/9 (11.1%)
2/8 (25.0%) 2/8 (25.0%) 0/8 (0%) 6/8 (75.0%)
4/7 (57.1%) 3/7 (42.9%) 1/7 (14.2~ 3/7 (42.9%)
1/2 (50.0%) 1/2 (50.0%) 0/2 (0%) 1/2 (50.0%)
20/22 (90.9%) 19/22 (86.4%) 1/22 (4.5%) 2/22 (9.1%)
12/15 (80.0%) 11/15 (73.3%) 1/15 (6.7%) 3/15 (20.0%)
7/9 (77.8%) 7/9 (77.8%) 0/9 (0%) 2/9 (22.2%)
7/8 (87.5%) 7/8 (87.5%) 0/8 (0%) 1/8 (12.5%)
6/7 (85.7%) 5/7 (71.4%) 1/7 (14.3%) ~ 1/7 (14.3%)
2/2 2/2 0/2 0/2
I - I I I IPL Abnormal Prolonged Disappear Normal I I I - V IPL Abnormal Prolonged Disappear Normal
(100.0% (100.0% (0%) (0%)
a Because of deafness due to Kawasaki's disease (case 9). N o r m a l BAEP was seen in only 1 case (case 15; Table 2). Abnormality of I - I I I I P L was recognized in 9 cases (prolongation in 8 cases and disappearance in I case). Abnormality o f I I I - V I P L was recognized in 20 cases (prolongation in 19 cases and disappearance in I case; Table 4). At the second examination in 15 cases with Chiari II m a l f o r m a t i o n (cases 1 - 1 5 ) , only I - I I I I P L prolongation was recognized in 2 cases (cases 1 and 8), only I I I - V I P L prolongation was recognized in 3 cases (cases 4, 6, and 7) and both I - I I I and I I I - V I P L prolongaltion were recognized in 8 cases (cases 2, 3, 5, 9, 10, 12, 13 and 14). Disappearance of waves III and V was recognized in one
case (case 11). In this case, only wave I was recognized. Each wave after wave II was absent. N o r m a l BAEP was seen in only one case (case 15; Table 2). Abnormality of I - I I I I P L was recognized in 11 cases (prolongation in 10 cases and disappearance in 1). Abnormality of I I I - V I P L was recognized in 12 cases (prolongation in 11 cases and disappearance in 1; Table 4). At the third examination in 9 cases with Chiari II m a l f o r m a t i o n (cases 1 - 9 ) , only I - I I I I P L prolongation was recognized in 2 cases (cases 4 and 8), only I I I - V I P L prolongation was recognized in 1 case (case 7), and both I - I I I and I I I - V I P L prolongation were recognized in 6 cases (cases 1, 2, 3, 5, 6 and 9). Disappearance of wave I,
320 Table 5. Summary of 7 cases with symptomatic Chiari type lI malformation with BAEP findings reported in the literature Type of onset Early onset type
Authors
Hayashi et al. [6] Holliday et al. [7]
Clinical symptoms
ABR
Level of spina bifida
Outcome
I - I I I IPL
I I I - V IPL
Normal
Bilateral prolongation Right prolongation; Light V disappears Bilateral V disappear III, IV, V disappear Right prolongation; Left V disappears
Lumbosacral Lumbosacral
Unknown
Lumbar
Unknown
Lumbar
Unknown
Lumbosacral
Improved
1
0 days
2
9 days
3
0 days
Stridor; respiratory disturbance Choking on feeding; spitting up; stridor; left facial nerve palsy; bilateral tongue fasciculation Stridor
4
0 days
Stridor
Bilateral prolongation Normal
Uematsu et al. [20]
5
1 month
Stridor
Normal
Our case [15]
6
2 months
Stridor
Normal
Bilateral prolongation
Lumbosacral
Dead
Stone et al. [18]
1
16 years
Occipitalgia; oscillopsia; horizontal double vision; dysarthria; weakness of lower extremities; truncal ataxia; mild ataxia in legs, etc.
Right II, III, disappear; left prolongation
Normal
Unknown
Improved
Nishimoto et al. [14]
Delayed onset type
Case Age
I I I and V was not recognized in any cases. N o r m a l BAEP was not seen in any cases (Table 2). A b n o r m a l i t y of 1 - I I I I P L was recognized in 8 cases (prolongation in 8 cases and disappearance in no cases). A b n o r m a l i t y of I I I - V I P L was recognized in 7 cases (prolongation in 7 cases and disappearance in no cases; Table 4). At the first examination in 8 cases without Chiari II m a l f o r m a t i o n (cases 23-30), 1-11I 1PL prolongation alone was not recognized in any case, I I I - V 1PL prolongation alone was recognized in 5 cases (cases 23, 24, 26, 29 and 30), and b o t h I - I I I and 111-V I P L prolongation were recognized in 2 cases (cases 25 and 28). Disappearance of waves 1, Ill and V was recognized in none of the cases. N o r m a l BAEP was seen in 1 case (case 27) (Table 2). Abnormality of I - I I I I P L was recognized in 2 cases (prolongation in 2 cases and disappearance in no case). Abnormality of I I I - V I P L was recognized in 7 cases (prolongation in 7 cases and disappearance in no cases; Table 4). At the second examination in 7 cases without Chiari II m a l f o r m a t i o n (cases 23-29), I - I I I I P L prolongation alone was not recognized in any cases, I I I - V I P L prolongation alone was recognized in 2 cases (cases 23 and 29), and both I - I I I and I I I - V I P L prolongation were recognized in 3 cases (cases 24, 27 and 28). Disappearance of waves I, I I I and V was recognized in one case (case 25) as a result of deafness due to K a w a s a k i ' s disease. N o r m a l BAEP was found in one case (case 26; Table 2). Abnormality of I - I I I I P L was recognized in 4 cases (prolongation in 3 cases and disappearance in 1). A b n o r m a l i t y of I I I - V I P L was recognized in 6 cases (prolongation in 5 cases and disappearance in 1; Table 4). At the third examination in 2 cases without Chiari II m a l f o r m a t i o n (cases 23 and 24), I - I I I I P L prolongation alone was not recognized in any case, I I I - V I P L prolon-
Left prolongation
Dead
gation alone was recognized in I (case 23), and b o t h I - I I I and 1 1 I - V I P L prolongation were recognized in 1 (case 24). Disappearance of waves I, II1 and V was recognized in no cases. N o r m a l BAEP was not found in any cases (Table 2). Abnormality of I - I I I I P L was recognized in 1 case (prolongation in 1 and disappearance in no cases). Abnormality of 11I-V 1PL was recognized in 2 cases (prolongation in 2 cases and disappearance in none; Table 4). In the patient with symptomatic Chiari I1 malformation (who suffered stridor), 111-V I P L was much prolonged, but 1 - 1 I I 1PL was within the normal range.
Chronological changes in BAEP findings In 22 cases, BAEP recordings were repeated after periods ranging f r o m 16 months to 7 years. There were 15 cases of a s y m p t o m a t i c Chiari II m a l f o r m a t i o n and 7 cases without Chiari II m a l f o r m a t i o n (Fig. 3). 1 - V I P L tended to shorten before 8 - 9 years of age. The shortening tendency was m o r e remarkable in the younger group. After 8 - 9 years of age, 1 - V I P L did not show any particular tendency. In some cases, it became prolonged and in some it was shorter (Fig. 4). W h e n 1 - V 1PL was divided into two parts, two rem a r k a b l e tendencies were clearly revealed. I - I I I I P L tended to be prolonged in comparison with the normal range (Fig. 5). On the other hand, I 1 1 - V I P L continued to decrease f r o m the prolonged to the normal range (Fig. 6). Although in 1 case (case 7), I - 1 I I I P L was shorter, the change was slight. I I 1 - V 1PL tended to shorten rapidly, especially before 1 year of age. I I I - V I P L continued to shorten until 25 years of age, which was much later than the age at which it should have com-
321
Latency (ms) 8.0"
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Fig. 3. Chronological change of latencies of waves I, III and V in 22 cases of meningomyelocele. 9 Chiari type II malformation ( + ) , o Chiari type II malformation ( - )
3.0
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change of I - V IPL in 22 cases of meningomyelocele. a Chiari type II malformation ( + ) , o Chiari type II malformation ( - )
9
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Fig. 5. Chronological change of I - I I I IPL in 22 cases of meningomyelocele. 9 Chiari type II malformation ( + ) , o Chiari type II malformation ( - )
322 | - V IPL
+ 2 S.D. mean
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Fig. 6. Chronological change of I I I - V IPL in 22 cases of meningo-
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Relationship between morphological abnormality on M R I and functional disorder on BAEP In 25 cases examined by MRI, the level of both IV ventricle and medulla oblongata were measured on the sagittal image. With regard to the degree of descent of the IV ventricle, the distance from the fastigium to the foramen magnum was measured (Fig. 1). The latencies of I, III and V waves and IPL of I - I I I and III V were compared with the two morphological parameters (Figs. 7-10). In 2 cases in which the degree of descent of the IV ventricle was remarkable (cases 11 and 12), the latency of wave V and I I I - V IPL were significantly prolonged (Figs. 9, 10), but generally no close relationship was found between morphological abnormality on M R I and functional disorder on BAEP. Tectum beaking, which is a typical feature in the midbrain when Chiari II malformation is present, was found
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in all 22 cases with Chiari II malformation. No close relationship was found between the presence of tectum beaking and BAEP findings.
Transition of BAEP findings after V-P shunt In 2 cases, BAEP recordings were investigated before and after shunt revision for shunt malfunction. Although each latency of waves III and V was shortened after the shunting operation, they were still prolonged compared to normal. Improvement of BAEP findings was based on the shortening of I I I - V IPL. The decrease in I - I I I IPL was only slight (Fig. 11). Discussion
Significance of I - I I I and I l I - V IPL in Chiari II malformation With regard to the origins of I - V waves on BAEP, Moller et al. [10] reported that the distal portion of the cochlear nerve is the origin of wave I, the proximal portion of this nerve is the origin of wave II, the cochlear nucleus wave III, the contralateral superior olivary nucleus wave IV, and the contralateral lateral lemniscus wave V. However, there is controversy regarding the details [4, 5, 10, 19]. As for the origin of wave III, the
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ipsilateral cochlear nucleus [10] described above, the contralateral superior olivary nucleus [4, 19], and the complex wave of the caudal portion of pons [5] have all been reported. Holliday et al. [7] considered I - III IPL to be the parameter that reflects stretching of the cochlear nerve. Stone et al. [18] considered I - I I I IPL to be the conduction time from the cochlear nerve to the caudal portion of the pons, that is to say, I - I I I IPL is thought to be a functional parameter of the peripheral portion of the auditory system. If the origin of wave II is regarded as the ipsilateral cochlear nucleus and that of wave III the contralateral superior olivary nucleus [4, 19], the conduction time of the caudal portion of the pons is contained in I - I I I IPL. This means that I - I I I IPL, strictly speaking, is not a functional parameter of the peripheral portion of the auditory system and that some indications of brainstem dysfunction may be reflected on I - I I I IPL. However, neuronal axons in the auditory pathway run horizontally in the caudal portion of the ports. Vertical stretching of the brain stem is thought to have little effect on it. Thus, we think that I - I I I IPL is mainly a parameter of cochlear nerve stretching. On the other hand, I I I - V IPL is a definite functional parameter of the upper brain stem, from the pons to the midbrain. After a shunting operation for hydrocephalus, I I I - V IPL was shortened, but I - I I I IPL was not shortened significantly. The latency of wave V was still prolonged compared to the control, which proves that there is brain stem dysfunction in the Chiari II malformation itself. Stone et al. [18] and Holliday et al. [7] reported that in Chiari II malformation, the dysfunction in the medullary
325 portion is reflected in I - I I I IPL better than in I I I - V IPL, but in this study, elongation of I - I I I IPL was mild. Abnormalities were found more frequently in I I I - V IPL than in I - I I I IPL. Short-latency somatosensory-evoked potentials on medial nerve stimulation (SEP), N9-N13 IPL was frequently found to be prolonged in cases in which I - I I I IPL was normal on BAEP (unpublished data). Ng-N13 IPL is the conduction time from the upper brachial plexus to the medulla oblongata. As to what this means, we think that only one part of medullary lesions, that causes stretching of the cochlear nerve, is reflected on I - I I I IPL on BAEP. Thus, even if I - I I I IPL is within the normal range, it may be a false-negative with regard to dysfunction in the medullary portion. In contrast, when I - I I I IPL is prolonged under conditions in which the cochlear nerve is markedly stretched, dysfunction may extend over the lower cranial nerves and medulla oblongata. No close relationship was found between the morphological abnormalities found on MRI and the functional disorders found on BAEP. This suggests that the brain stem functional disorders in Chiari II malformation do not always correlate closely with the degree of anatomical anomaly. Dysfunctions that have no relationship to the morphological abnormality of the Chiari II malformation may exist in the brain stem. The degree of dysfunction varies intrinsically from case to case. In some cases without Chiari II malformation, I I I - V IPL was prolonged significantly. This may suggest the existence of a functional disorder in the brain stem of the meningomyelocele itself (both with and without Chiari II malformation). Therefore, new functional disorders, compatible with the degree of morphological abnormality, may be added to this intrinsic dysfunction after birth.
Natural history of the Chiari H malformation Chronological changes on BAEP showed two remarkable tendencies. In the first place, I I I - V IPL continued to decrease from prolonged to the normal range with growth. Secondly, I - I I I IPL tended to be prolonged gradually from the normal range. These findings may indicate that the natural history of Chiari II malformation is delayed maturation of the brain stem and intensification in stretching of the cochlear nerve. Stretching of t h e cochlear nerve is considered to coexist in most cases with elongation and stretching of other lower cranial nerves and the hindbrain. With regard to the development of the auditory system in the normal human, the following findings have been reported. Although the cochlear nerve is already myelinated at birth, myelination of the auditory system in the brain stem occurs later than in its peripheral portion. It reaches the medial geniculate body at 6 months of age and the auditory cortex at 12 months. The latency of wave I shortened to the range of that in adults at 2 months of age, that of wave III at 2 years, and that of wave V at 3 years on BAEP [9]. There is a time lag between anatomical development in the auditory system and functional maturation on BAEP.
Inagaki et al. [8] reported auditory system maturation by using other parameters. They reported pontine auditory conduction velocity (PACV) as a functional parameter and each neuron density in the cochlear nucleus and in the inferior colliculus as morphological parameters. PACV reaches the adult value by 2 - 4 years of age, and neuron density decreases to the adult value by 32-33 weeks of viviparous in inferior colliculus and by 2 - 4 months of age in cochlear nucleus. Thus, functional maturation of the auditory system in the brain stem is thought to be completed by 3 - 4 years of age in the normal human being. The mechanism of delayed maturation in the brain stem of Chiari II malformation is unknown. Myelination is disturbed in some part of the brain stem of children with Chiari II malformation [14, 16]. Either the degree or the speed of myelination may be delayed compared to the normal range.
Prognostic value of BAEP in Chiari H malformation In 7 cases, BAEP findings have been reported in symptomatic Chiari II malformation, including one of our cases (Table 5) [6, 7, 14, 15, 18, 20]. In 6 cases of early-onset type [6, 7, 14, 15, 20], I I I - V IPL was abnormal in all cases, but I - I I I IPL was abnormal in only 2 cases. On the other hand, in 1 case of delayed-onset type [18], I - I I I IPL was abnormal and I I I - V IPL normal. "Abnormal" means either wave disappearance or prolongation of latencies. Nishimoto et al. [14] pointed out the disappearance of wave V as a strong indicator of clinical onset. They reported that cases had no clinical symptoms if BAEP findings were normal or latencies of each wave were only prolonged. On the other hand, Holliday et al. [7] found no significant difference of BAEP between symptomatic and asymptomatic cases in a single examination. They suggested the possibility that repeated investigations would reveal the differences in BAEP findings between symptomatic and asymptomatic cases. Abnormalities in I I I - V IPL recognized in early-onset cases reveal the dysfunction that exists in the upper brain stem from the pons to midbrain. They do not always correlate closely with the severity of the Chiari II anomaly. Dysfunction that is intrinsic in the brainstem of Chiari II malformation is thought to be reflected on I I I - V IPL. This primary dysfunction, reflected on I I I - V IPL, may involve not only the upper brain stem but the entire brain stem. In cases with prolongation of I I I - V IPL or disappearance of III to V waves on BAEP, dysfunctions that are compatible with the degree of I I I - V IPL abnormality may also involve the medulla oblongata. In these cases, only a slight alteration in the factors acting on the hindbrain may readily precipitate symptoms. On the other hand, in cases in whom the intrinsic dysfunction is mild, that is, minimal abnormality in I I I - V IPL, the children grow up without symptoms as long as this is below the threshold. Meanwhile the delayed maturation is slowly progressing in the brainstem.
326 At the same time, elongation and stretching in the medulla oblongata and lower cranial nerves intensify with growth. Patients in w h o m I - I I I I P L rapidly prolongs or I to III waves disappear on BAEP become symptomatic, as the delayed-onset type, when the threshold is exceeded. In the early-onset type, suboccipital decompression does not always bring a b o u t an i m p r o v e m e n t in clinical symptoms. I f anything, in m o s t cases the outcome is worsened. In these cases, the result proves that the cause of clinical s y m p t o m s cannot be overcome by decompression of the medullary portion. It suggests, instead, the existence of a certain functional disorder that basically has no relationship with the morphological aspects. As intraoperative findings in delayed onset types, Benerji [2] reported that the medulla oblongata is fixed to the cervical vertebrae by arachnoid-dural bands. This m a y strongly support the suggestion that secondary factors have something to do with the delayed onset. In the delayed-onset type, results of suboccipital decompression are better than in the early-onset type [2, 17], suggesting that the cause of delayed onset is mechanical compression. As mechanisms of clinical onset of the Chiari II malformation, the following have been reported: (1) primary brain stem dysfunction; (2) secondary disorders such as compression of brain stem and lower cranial nerves by descended cerebellar tonsils, stretching of lower cranial nerves by cervicomedullary kinking, strangulation by fibrous arachnoid-dural bands, pressure imbalance between intracranial and intraspinal cavities, disturbance of blood circulation by deviation of vertebral-basilar arteries. The mechanism is not single and simple. Several factors are combined at the onset. BAEP cannot directly reveal the focus in the medulla oblongata responsible for the Chiari II s y m p t o m s because of the anatomical confines of the auditory system. Although the pathological state reflected by BAEP is only a part o f the Chiari II malformation, the primary factors are mainly reflected in I I I - V I P L on BAEP, and the secondary factors are partly reflected in I - I I I IPL. Patients in w h o m BAEP shows a significant degree of I I I - V I P L abnormality are very likely to present as the early-onset type. Some o f the secondary factors m a k e I - I I I I P L a b n o r m a l when the cochlear nerve is stretched. I f I - I I I I P L rapidly becomes a b n o r m a l during growth, the patients are very likely to be of the delayed-onset type. Only one symptomatic case was included in the present study, so quantitative analysis on BAEP findings cannot be discussed f r o m the point of view of clinical onset. Instead quantitative analysis with regard to the clinical onset should be investigated. To evaluate dysfunction of the medulla oblongata and lower cranial nerves, B A E P alone is insufficient although it is superior to SEP because o f the simplicity of the investigation technique. It is better to combine it with SEP and blink reflex. We do not have enough control data yet in SEP in normal newborns and infants. We are of the opinion that evaluation of medullary function by SEP and blink reflex will reveal m o r e details a b o u t pathological states in the Chiari I I malformation. We are presently accumulating such data.
Acknowledgement. The authors would like to record here their warm gratitude to Patrick Eghwrudjakpor, M.D., for proofreading this paper and Sueo Eguchi, M.D., for taking care of the patients at a center for handicapped children in Kochi. References 1. Arnold J (1894) Myelocyste, Transposition von Gewebskeimen und Sympodie. Beitr Pathol Anat 16:1-28 2. Benerji NK, Miller HD (1974) Chiari malformation presenting in adult life. Its relationship to syringomyelia. Brain 97: 157168 3. Chiari H (1891) Lrber Verfinderungen des Kleinhirns infolge yon Hydrocephalie des Grosshirns. Dtsch Med Wochenschr 17:1172-1175 4. Hashimoto I (1985) Auditory brainstem responses (in Japanese). Brain Nerve 37:871-887 5. Hashimoto I, Ishiyama Y, Yoshimoto T, Nemoto S (1981) Brain stem auditory evoked potentials recorded directly from human brain stem and thalamus. Brain 104:841-859 6. Hayashi T, Moritaka K, Kuramoto S (1984) Clinical application of auditory brainstem response in neonates and children (English abstract). Clin Electroencephalogr 26:153-164 7. Holliday PO, Pillsbury D, Kelly DL Jr, Dillar JR (1985) Brainstem auditory evoked potentials in Arnold-Chiari malformation: possible prognostic value and changes with surgical decompression. Neurosurgery 16:48-53 8. Inagaki M, Tomita Y, Tadashima S, Ohtani K, Andoh G, Takeshita K (1987) Functional and morphometrical maturation of the brainstem auditory pathway. Brain Dev 9:597-601 9. Matsuzawa K, Seki S, Fujita H, Shimizu S, Honma T (1981) Developmental changes of auditory brainstem responses and their application to electrical response audiometry (English abstract) (in Japanese). No To Hattatsu 13:318-328 10. Moller AR, Jannetta PJ (1983) Auditory evoked potentials recorded from the cochlear nucleus and its vicinity in man. J Neurosurg 59:1013-1018 11. Mori K (1985) Anomalies of the central nervous system. Thieme-Stratton, New York, pp 97-109 12. Mori K, Handa H, Okuno T, Hazama F (1978) Arnold-Chiari type II malformation: a clinicopathological study with special reference to its surgical treatment. Neurochirurgia 21:9-14 13. Mori K, Uchida Y, Nishimura T, Eghwrudjakpor OP (1988) Brain stem auditory evoked potentials in Chiari-II malformation. Child's Nerv Syst 4:154-157 14. Nishimoto H, Kagawa Y, Maeda K, Tsukiyama T, Tsubokawa T (1986) Evaluation of auditory brainstem response in children with myelomeningocele (English abstract) (in Japanese). Nerv Syst Child 11: 407-413 15. Nishimura T, Mori K, Uchida Y, Ohira T, Kamimura Y (1988) Evaluation of brainstem dysfunction by auditory brainstem response in patients with myelomeningocele - follow-up studies for two months to five years (English abstract) (in Japanese). Nerv Syst Child 13:445-456 16. Peach B (1965) Arnold-Chiari malformation. Anatomic features of 20 cases. Arch Neurol 12:613-621 17. Saez RJ, Onofrio BM, Yanagihara T (1976) Experience with Arnold-Chiari malformation, 1960 to 1970. J Neurosurg 45:416-422 18. Stone JL, Bouffard A, Morris R, Hovsepian W, Mayers HL (1983) Clinical and electrophysiologic recovery in ArnoldChiari malformation. Surg Neurol 20:313- 317 19. Tsuji S (1986) Brainstem auditory evoked potentials in cases with brainstem lesions (English abstract) (in Japanese). Adv Neurol Sci 30:350-359 20. Uematsu Y, Kuwata T, Iwamoto M, Kuriyama T (1987) Arnold-Chiari malformation with successful posterior fossa decompression in an infant - with emphasis on significance of auditory brainstem response (English abstract) (in Japanese). Nerv Syst Child 12:465-570
