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Prediction and evaluation of brainstem function by auditory brainstem responses in patients with uncal herniation
Surg Neurol
81
1987;27:81-6
Prediction and Evaluation of Brainstem Function by Auditory Brainstem Responses in Patients with Uncal Herniation Seigo N a g a o , M . D . , H i d e y u k i K u y a m a , M.D., Y u t a k a H o n m a , M.D., Fumiyuki Momma, M.D., Tsukasa Nishiura, M.D., Takenobu Murota, M.D., M a s a k a z u Suga, M . D . , T a k a h o T a n i m o t o , M . D . , M a s a m i t s u K a w a u c h i , M . D . , a n d Akira Nishimoto, M.D. Department of Neurological Surgery, Okayama University Medical School, Okayama, Japan
Naga0 S, Kuyarna H, Honma Y, Momma F, Nishiura T, Murota T, Suga M, Tanimoto T, Kawauchi M, Nishimoto A. Prediction and evaluation of brainstem function by auditory brainstem responses in patients with uncal herniation. Surg Neurol 1987;27:81-6.
Serial measurements of auditory brainstem-evoked responses (BERs) were conducted in 15 patients with supratentorial mass lesions, Significant prolongation of the latency of wave V BERs, which originates in the inferior c011iculus, occurred when the intracranial pressure (ICP) approached 30 mmHg. In four of five patients whose BERs were measured before pupillary changes, a significant lengthening of wave V latency was observed prior to clinical manifestation of uncal herniation. These results suggest that immediate medical or surgical decompression Of ICP should be performed when ICP approaches 30 mmHg with significant prolongation of wave V latency. KEY WORDS: Intracranial pressure; Uncal herniation; Auditory
brainstem response; Brainstem
Early detection of uncal herniation in patients with supratentorial space-occupying lesions is essential for reducing morbidity and mortality. One author [5] has reported that changes in wave V auditory brainstemevoked responses (BERs), which originate predominantly in the inferior colliculus [3], could indicate early changes in the brainstem function and predict uncal herniation, and assess the effectiveness of decompression procedures in experimentally produced supratentorial expanding lesions [9,10]. In clinical cases, we have already confirmed that an increase in the latency and deterioration of the wave V BERs correlated well with the rostrocaudal neurological impairment of uncal herniation defined by Plum and Posner [12], especially after Address reprint requests to: Seigo Nagao, M.D., Department of Neurological Surgery, Okayama University Medical School, 2-5-1, Shikata-cho, Okayama, 700, Japan.
© |987 by ElsevierSciencePublishingCo., Inc.
the appearance of pupillary abnormalities [11]. In this article, we have studied whether measurements of wave V BERs can predict critical upper brainstem dysfunction before the appearance of pupillary abnormalities and whether it can indicate the effectiveness of medical decompression of intracranial pressure (ICP) on the brainstem function in the stage of pupillary abnormality.
Materials and Methods The BERs of 15 patients with supratentorial mass lesions (nine men and six women, aged 22-72 years) were recorded. There were nine cases of brain tumor, two cases of intracerebral hematoma, and four cases of massive cerebral infarction by cerebral vasospasm because of subarachnoid hemorrhage. All cases presented clinical signs of uncal herniation in the course of therapy. The patient was lying supine in a quiet room. Electroencephalographic needle electrodes were attached at the vertex and at both mastoids. Auditory clicks of 115 dB, 0.1 ms duration, were delivered monaurally through shielded headphones at a rate of 10 per second. Bipolar electroencephalographic activity was recorded from the vertex and the mastoid ipsilateral to stimulation, with the contralateral mastoid serving as ground. This signal was amplified 5 × 105 times (bioelectric amplifier 3G26, Nihondenki-San-Ei Instrument Co., Tokyo, Japan) with a filter bandpass of 100"3000 Hz. The computer average of 1000 such responses was obtained twice from each ear and was recorded on an X - Y plotter (signal processor 7T08, Nihondenki-San-Ei Instrument Co.). All recordings were completed within 20 minutes. The latencies from the stimulus to the positive peak of wave V and III-V interwave latencies were measured. As wave III BERs originate in the superior olivary complex, III-V interwave latencies represent the brainstem conduction time. In the following results, "mass side" BERs refers to the BERs recorded from the vertex to the mass0090-3019/87/$3.50
82
Surg Neurol 1987;27:81-6
Nagao et al
for 3 - 1 0 days by a pressure transducer (epidural transducer, model P-16S, Telemex, Inc., Tokyo) in the extradural space. All ICP values were expressed as the mean. For ICP decompression, 200 ml of 10% glycerol solution was administered intravenously over a 3 0 - 4 0 minute period. The decompression effect was evaluated by comparing the changes in the wave V and I I I - V BER interwave latencies immediately before administration and at the lowest point of ICP.
Table 1. Latency of Auditory Brainstem Responses in 20 Adult Subjects Wave
1
II
Ill
IV
V
M e a n (ms/ SD
1.35 0.08
2.48 0.14
3.60 0.13
4.78 0.12
5.50 0.15
IlI-V
1.90 0.16
SD indicates standard deviation (n - 20).
side mastoid lead stimulating the ipsilateral ear. "Contralateral" means non-mass-side BERs.
Results
Data from 20 healthy volunteers (13 men and 7 women; aged 2 0 - 3 3 years) served as controls. In 5 out of 15 patients, measurements of BERs were started 3 - 4 8 hours before pupillary changes. In six patients who progressed to the third nerve paralysis stage, defined by Plum and Posner [12], the prolongation of wave V and I I I - V BER interwave latencies were correlated with changes in ICP and normalization of dilated pupils before and after administration of hypertonic solution. Intracranial pressure was measured consecutively
Table 1 gives the latencies of waves I - V and the interwave latency of wave I I I - V in 20 healthy subjects in our department; the results agree fairly well with reports from other institutions. Wave V and I I I - V interwave latencies were considered abnormal if the latencies exceeded the mean + 2 SD, i.e., ->5.80 ms in wave V and ->2.22 ms in I I I - V interwave latency. The wave V and I I I - V interwave latencies were plotted against ICP in 15 patients (Figure 11. It can be seen
ICP mmM!
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:
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".
•
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5.0
5.2
5.4
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F i g u r e 1. Composite plot of relationship between wave
5.8
6.0
6.2
6.4
6.6
6.8 m,,c
W a v e V Latency ICP mmHg
6O
5O
•
O
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1.2
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2.2
2.4
2.6
2.8
3.0
3.2 m,,c
] I I - V I n t e r w a v e Latency
V and I I I - V interwave latencies and increased intracranial pressure (ICP). Horizontal and vertical solid lines indicate l 5 mmHg of ICP and the normal upper limit of latencies. Inconsistent latency prolongation occurs in II1-V interwave latencies during intracranial hypertension.
Brainstem Response and Uncal Herniation
Surg Neurol 1987;27:81-6
Pul)iHary change (-)
Right frontal tumor 6 2 F ICP
mmHg
3O,
I
i
i 10,
Figure 2. Intracranial pressure (ICP) and au-
83
;
'
'
I
! m
30mln
ditory brainstem-evoked responses (BERs) recorded from a 62-year-old woman with a right frontal glioma, showing a significant increase in the latency of wave V with elevation of lCP. The patient did not show anisocoria.
O'
i
l
,
BER
5.64
5.95
i
lpv
2 msec
that increases in ICP do not necessarily result in prolongation of the latency, especially with the III-V interwave latency. However, for wave V, significantly prolonged latencies were observed in patients with high ICPs over 15 mmHg. At ICPs of -~30 mmHg, the wave V latency approached the upper limit of the normal range or became significantly prolonged. In Figure 2, changes in |CP and BERs are shown in a patient with right frontal glioma. The latency of mass-
m
m
c e Jr-
Figure 3. Serial changes in wave V and III-V interwave latencies before pupillary changes in five patients. Solid and dashed lines indicate "mass side" and "contralateral" auditory brainstem responses, respectively (see text). Thick vertical solid lines indicate the upper limit of wave V and III-V interwave latencies.
side wave V BERs was normal at an ICP of 15 mmHg (left). Three hours later, the ICP increased to 25-30 mmHg, presumably because of respiratory problems, with significant prolongation of the wave V latency (right). The pupils were isocoric and reacted normally to light. Three hours after measurement of BERs, the patient's consciousness deteriorated and the pupils became anisocoric; the diagnosis of early third-nerve stage of uncal herniation was made, as defined by Plum and Posner
15
0 ......
;
mass side
:
c o n t r a l s t e r s l side
D
'5. 0,.
10-
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0 X
5
~
$
2 ]]l-V Interwave Latency
"/.
3
~
5
_~*~
~w
~_
6 Wave V Latency
~
,
7 msac
84
Surg Neurol 1987;27:81-6
Nagao et al
Cerebral Infarction
latency in 24 of 27 measurements. However, pupillary normalization was observed on only five occasions (solid circles). Thus, in a large number of the measurements, shortening (normalization) of wave V latencies was observed without clinical improvement of uncal herniation. Less consistent results were indicated in the changes ill I I I - V interwave latencies.
mmHg 110% Glycerol 50
M
Discussion
20, 10. Early IIIrd nerve stage before
1 pv ÷ 0
5
10 msec
Figure 4. Effect of decompression of intracranla/ pressure on the/ateno' of wave V auditory brainstem-evoked responses in a patient with anisocoria due to massive cerebral infarction.
[12]. Thus, a significant change in the latency of wave V preceded the clinical manifestation of uncal herniation in this patient. Sequential changes in the wave V and I I I - V interwave latencies are shown in five patients, whose BERs were measured 3 - 4 8 hours before pupillary changes (Figure 3). On the mass-side BERs, one patient showed abnormal wave V and I ! I - V interwave latencies prior to pupillary changes. In the contralateral BERs, however, four patients exhibited upper limit of normal, or abnormal, wave V latencies 2-15 hours prior to pupillary change. The III-V interwave latencies were abnormal in two patients 4 - 1 0 hours before uncal herniation. Only one patient had normal wave V and III-V interwave latencies for 5 hours in both side BERs before pupillary changes. The effect o f medical decompression of ICP on BERs was illustrated in one patient with anisocoria resulting from massive cerebral infarction (Figure 4). The prolonged latency of wave V (5.98 ms) became normal (5.44 ms) after the ICP decreased from 34 to 16 m m H g with normalization of pupils. Figure 5 summarizes the effects of a decrease in ICP on wave V and I I I - V interwave latencies in patients with uncal herniation manifesting pupillary abnormalities. A decrease in ICP with 10% glycerol solution resulted in shortening of the wave V
In uncal herniation with supratentorial mass lesions, first the rostral midbrain is compressed directly by the herniated brain, and then the dorsal surface of the brainstem, including the inferior colliculus, is displaced caudally more than its ventral surface [6,14]. At the same time, mechanical compression of the upper brainstem causes interference with circulation of the inferior colliculus in the early stage [4]. With this pathophysiological background of uncal herniation, Nagao et al [9,10] reported that changes in the latency and wave form of wave V BERs, which originates predominantly in the inferior colliculus, could indicate early changes of the brainstem function and predict uncal herniation in acute supratentorial expanding lesions. Pupillary change has been shown to be one of the earliest clinical signs of uncal herniation in supratentorial mass lesions. Munro and Sisson [8], however, reported that pupillary changes were not observed in 50% of the patients with uncal herniation verified by autopsy. The main causes for the discrepancy in the clinical manifestation and severity of uncal herniation have been attributed to individual anatomic differences, such as the size and configuration of the tentorial hiatus, the third nerve pathway, the direction of herniated brain, and the displaceable capacity of the brainstem. In these patients, medical or surgical decompression of ICP should be started prior to pupillary changes with the aid of an objective assessment of upper brainstem function. We employed the BERs for this purpose. York et al [ 16] reported a linear relationship between an increase in latency of wave N2 (70 ms) of the visualevoked responses and elevated ICP in patients with hydrocephalus and with cerebral edema. They also showed that, when the N2 latency increased to 90 ms, the ICP increased to a critical level around 400 m m H 2 0 (30 mmHg) [ 15,16]. Significant increases in the latency of wave V BERs and in the central conduction time of the brainstem auditory pathway were indicated in experimentally increased ICP produced by extradural balloon compression [9] and cerebrospinal fluid infusion to the lateral ventricle [7]. Benna et al [2] have documented BER abnormalities consisting of increases in wave I I I - V and I - V latency conduction times and amplitude reductions of wave V in patients with supratentorial tu-
Brainstem Response and Uncal Herniation
Surg Neurol 1987;27:81-6
85
ICP mmHg
70
60
/ /
50
/
Y
40 30 20 10
Figure 5. Changes in the wave V and I I I - V interwat,e latencies by lowering intracranial pressure (ICP) in patients with uncal herniation. Large solid circles indicate normalization of pupillary abnormality. Decrease in ICP resulted in shortening or normalization of the latency of wave V without significant clinical improvement in most of the trials. Inconsistent changes in the I I I - V interwave latencies were obtained.
o
5.0
5.2
5.4
5.6
5.8
6.0
6.2
6.4
6.6
6.8 m=ec
Wave V Latency
ICP mmHg
6O
5O
40
30
20
l0
0 1,2
1.4
1.6
1.8
2.0
•
2.2
2.4
2.6
2.8
3.0 mzec
I I ] - V Interwave Latency
mors who showed clinical signs of increased ICP [2]. However, they did not show the ICP values. Our results show that the latency o f wave V was significantly prolonged even at an ICP o f 20 mmHg. At ICPs o f 30 m m H g , it approaches the upper limit o f the normal value (5.8 ms) or becomes significantly prolonged. Inconsistent latency prolongation occurs in the I I I - V interwave latencies. In head injured patients, Tsubokawa et al [13] showed that prolonged latency or disappearance o f wave V was observed in some cases without brainstem symptoms, and indicated that the BER would provide an early diagnosis of brainstem dysfunction, even when neurological signs are not yet apparent [13]. Ahmed [1] also reported prolongation of I - V interwave latencies in cases of uncal herniation and felt that the changes in the BERs
were noted earlier than clinically seen. In our data with gradual supratentorial expanding lesions, the latency of wave V became abnormal 2 - 1 5 hours before pupillary changes in four of five patients, especially in the "contralateral" BERs. Similar results were reported by Benna et al [2], where four patients had BER abnormalities only on the same side of the tumor, and four patients also showed abnormalities contralaterally. Therefore, it should be emphasized that bilateral measurements of BERs are essential in patients with increased ICP. These facts strongly indicate that in patients with supratentorial mass lesions, the upper brainstem function is critical when ICP approaches 30 mmHg, with significant prolongation o f wave V latency. In this situation, intensive medical or surgical decompression to relieve the ICP should be performed as soon as possible. We have shown
86
Surg Neurol 1987;27:81-6
a reversible change in the latency and amplitude o f wave V in cats that have undergone decompression to alleviate ICP [9]. In our clinical experience, the use o f hypertonic solution to decrease ICP resulted in the shortening or normalization o f the wave V latency in almost all patients with anisocoria. H o w e v e r , pupillary normalization was only observed in 5 o f 27 trials in which decompression was used. In patients without pupillary normalization, or in patients w h o remained clinically unchanged, the effectiveness o f medical decompression o f ICP is obscure, and it is often hard to decide whether or not medical decompression is sufficient for recovery o f brainstem function, and whether or not the same treatment should be continued. Measurement o f wave V BERs seems to provide objective parameters that can be used to assess the effectiveness o f ICP decompression on the brainstem.
The authors gratefully acknowledge the suggestions and revisions of Dr. Robert A. Moody, Chairman of Neurosurgery, Guthrie Clinic, Sayre, Pennsylvania, and Miss Keiko Tanida for preparing the manuscript.
References 1. Ahmed 1. Brain stem auditory evoked potentials in transtentorial herniation. Clin Electroencephalogr 1980;11:34-7. 2. Benna P, Gilli M, Ferrero P, Bergamasco B. Brain stem auditory evoked potentials in supratentorial tumors. Electroencephalogr Clin Neurophysiol 1982;54:8-9. 3. Buchwald JS, Huang C-M. Far-field acoustic response. Origins in the cat. Science 1975;189:382-4. 4. Goodman SJ, Becker DP. Vascular pathology of the brain stem due to experimentally increased intracranial pressure. Changes
Nagao et al
noted in the micro- and macrocirculation. J Neurosurg 1973;39:601-9. 5. Jewett DL. Volume-conducted potentials in response to auditory stimuli as detected by averaging in the cat. Electroencephalogr Clin Neurophysiol 1970;28:609-18. 6. Johnson RT, Yates PD. Brain stem hemorrhage in expanding supratentorial conditions. Acta Radiol (Diagn) 1956;46:250-6. 7. McPherson D, Blanks J, Foltz E. Intracranial pressure effects on auditory evoked responses in the rabbit. Preliminary report. Neurosurgery 1984;14:161-6. 8. Munro D, Sisson WR Jr. Hernia through the incisura of the tentorium cerebelli in connection with craniocerebral trauma. N Engl J Med 1952;247:699-708. 9. Nagao S, Roccaforte P, Moody RA. Acute intracranial hypertension and auditory brain-stem responses. Part i: changes in the auditory brain-stem and somatosensory evoked responses in intracranial hypertension in cats. J Neurosurg 1979;51:669-76. 10. Nagao S, Roccaforte P, Moody RA. Acute intracranial hypertension and auditory brain-stem responses. Part 2: the effects of brain-stem movement on the auditory brain-stem responses due to transtentorial herniation. J Neurosurg 1979;5 l:846-51. l 1. Nagao S, Sunami N, Tsutsui T, Honma Y, Fujimoto S, Ohmoto T, Nishimoto A. Serial observation of brain-stem function in acute intracranial hypertension by auditory brain-stem responses--a clinical study, ln: Ishii S, Nagai H, Brock M, eds. lntracranial pressure. Vol. 5. Berlin, Heidelberg, New York, Tokyo: SpringerVerlag, 1983:474-9. 12. Plum F, Posner JB. The diagnosis of stupor and coma. 3rd ed. Philadelphia: FA Davis, 1980;109-11. 13. Tsubokawa T, Nishimoto H, Yamamoto T, Kitamura M, Katayama Y, Moriyasu N. Assessment of brainstem damage by the auditory brainstem response in acute severe head injury. J Neurol Neurosurg Psychiatry 1980;43:1005-1 l. 14. Weinstein JD, Langfitt TW, Bruno L, Zaren HA, Jackson LF. Experimental study of patterns of brain distortion and ischemia produced by an intracranial mass. J Neurosurg 1968;28:513-21. 15. York DH, Pulliam MW, Rosenfeld JG, Watts C. Relationship between visual evoked potentials and intracranial pressure. J Neurosurg 1981;55:909-16. 16. York D, Legan M, Benner S, Watts C, Further studies with a noninvasive method of intracranial pressure estimation. Neurosurgery 1984;14:456-61.
81
1987;27:81-6
Prediction and Evaluation of Brainstem Function by Auditory Brainstem Responses in Patients with Uncal Herniation Seigo N a g a o , M . D . , H i d e y u k i K u y a m a , M.D., Y u t a k a H o n m a , M.D., Fumiyuki Momma, M.D., Tsukasa Nishiura, M.D., Takenobu Murota, M.D., M a s a k a z u Suga, M . D . , T a k a h o T a n i m o t o , M . D . , M a s a m i t s u K a w a u c h i , M . D . , a n d Akira Nishimoto, M.D. Department of Neurological Surgery, Okayama University Medical School, Okayama, Japan
Naga0 S, Kuyarna H, Honma Y, Momma F, Nishiura T, Murota T, Suga M, Tanimoto T, Kawauchi M, Nishimoto A. Prediction and evaluation of brainstem function by auditory brainstem responses in patients with uncal herniation. Surg Neurol 1987;27:81-6.
Serial measurements of auditory brainstem-evoked responses (BERs) were conducted in 15 patients with supratentorial mass lesions, Significant prolongation of the latency of wave V BERs, which originates in the inferior c011iculus, occurred when the intracranial pressure (ICP) approached 30 mmHg. In four of five patients whose BERs were measured before pupillary changes, a significant lengthening of wave V latency was observed prior to clinical manifestation of uncal herniation. These results suggest that immediate medical or surgical decompression Of ICP should be performed when ICP approaches 30 mmHg with significant prolongation of wave V latency. KEY WORDS: Intracranial pressure; Uncal herniation; Auditory
brainstem response; Brainstem
Early detection of uncal herniation in patients with supratentorial space-occupying lesions is essential for reducing morbidity and mortality. One author [5] has reported that changes in wave V auditory brainstemevoked responses (BERs), which originate predominantly in the inferior colliculus [3], could indicate early changes in the brainstem function and predict uncal herniation, and assess the effectiveness of decompression procedures in experimentally produced supratentorial expanding lesions [9,10]. In clinical cases, we have already confirmed that an increase in the latency and deterioration of the wave V BERs correlated well with the rostrocaudal neurological impairment of uncal herniation defined by Plum and Posner [12], especially after Address reprint requests to: Seigo Nagao, M.D., Department of Neurological Surgery, Okayama University Medical School, 2-5-1, Shikata-cho, Okayama, 700, Japan.
© |987 by ElsevierSciencePublishingCo., Inc.
the appearance of pupillary abnormalities [11]. In this article, we have studied whether measurements of wave V BERs can predict critical upper brainstem dysfunction before the appearance of pupillary abnormalities and whether it can indicate the effectiveness of medical decompression of intracranial pressure (ICP) on the brainstem function in the stage of pupillary abnormality.
Materials and Methods The BERs of 15 patients with supratentorial mass lesions (nine men and six women, aged 22-72 years) were recorded. There were nine cases of brain tumor, two cases of intracerebral hematoma, and four cases of massive cerebral infarction by cerebral vasospasm because of subarachnoid hemorrhage. All cases presented clinical signs of uncal herniation in the course of therapy. The patient was lying supine in a quiet room. Electroencephalographic needle electrodes were attached at the vertex and at both mastoids. Auditory clicks of 115 dB, 0.1 ms duration, were delivered monaurally through shielded headphones at a rate of 10 per second. Bipolar electroencephalographic activity was recorded from the vertex and the mastoid ipsilateral to stimulation, with the contralateral mastoid serving as ground. This signal was amplified 5 × 105 times (bioelectric amplifier 3G26, Nihondenki-San-Ei Instrument Co., Tokyo, Japan) with a filter bandpass of 100"3000 Hz. The computer average of 1000 such responses was obtained twice from each ear and was recorded on an X - Y plotter (signal processor 7T08, Nihondenki-San-Ei Instrument Co.). All recordings were completed within 20 minutes. The latencies from the stimulus to the positive peak of wave V and III-V interwave latencies were measured. As wave III BERs originate in the superior olivary complex, III-V interwave latencies represent the brainstem conduction time. In the following results, "mass side" BERs refers to the BERs recorded from the vertex to the mass0090-3019/87/$3.50
82
Surg Neurol 1987;27:81-6
Nagao et al
for 3 - 1 0 days by a pressure transducer (epidural transducer, model P-16S, Telemex, Inc., Tokyo) in the extradural space. All ICP values were expressed as the mean. For ICP decompression, 200 ml of 10% glycerol solution was administered intravenously over a 3 0 - 4 0 minute period. The decompression effect was evaluated by comparing the changes in the wave V and I I I - V BER interwave latencies immediately before administration and at the lowest point of ICP.
Table 1. Latency of Auditory Brainstem Responses in 20 Adult Subjects Wave
1
II
Ill
IV
V
M e a n (ms/ SD
1.35 0.08
2.48 0.14
3.60 0.13
4.78 0.12
5.50 0.15
IlI-V
1.90 0.16
SD indicates standard deviation (n - 20).
side mastoid lead stimulating the ipsilateral ear. "Contralateral" means non-mass-side BERs.
Results
Data from 20 healthy volunteers (13 men and 7 women; aged 2 0 - 3 3 years) served as controls. In 5 out of 15 patients, measurements of BERs were started 3 - 4 8 hours before pupillary changes. In six patients who progressed to the third nerve paralysis stage, defined by Plum and Posner [12], the prolongation of wave V and I I I - V BER interwave latencies were correlated with changes in ICP and normalization of dilated pupils before and after administration of hypertonic solution. Intracranial pressure was measured consecutively
Table 1 gives the latencies of waves I - V and the interwave latency of wave I I I - V in 20 healthy subjects in our department; the results agree fairly well with reports from other institutions. Wave V and I I I - V interwave latencies were considered abnormal if the latencies exceeded the mean + 2 SD, i.e., ->5.80 ms in wave V and ->2.22 ms in I I I - V interwave latency. The wave V and I I I - V interwave latencies were plotted against ICP in 15 patients (Figure 11. It can be seen
ICP mmM!
70
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i
"
5O
4O
o ~
o~
•
•
I •
3O
eo
ao
•
•e
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• •
oo
.:
:
". •
".
•
•.
2O
10
0
•
5.0
5.2
5.4
1
5.6
F i g u r e 1. Composite plot of relationship between wave
5.8
6.0
6.2
6.4
6.6
6.8 m,,c
W a v e V Latency ICP mmHg
6O
5O
•
O
4O
u
3O
•
w
•
•
2O
10
0
1.2
1.4
1.6
1.8
2.0
2.2
2.4
2.6
2.8
3.0
3.2 m,,c
] I I - V I n t e r w a v e Latency
V and I I I - V interwave latencies and increased intracranial pressure (ICP). Horizontal and vertical solid lines indicate l 5 mmHg of ICP and the normal upper limit of latencies. Inconsistent latency prolongation occurs in II1-V interwave latencies during intracranial hypertension.
Brainstem Response and Uncal Herniation
Surg Neurol 1987;27:81-6
Pul)iHary change (-)
Right frontal tumor 6 2 F ICP
mmHg
3O,
I
i
i 10,
Figure 2. Intracranial pressure (ICP) and au-
83
;
'
'
I
! m
30mln
ditory brainstem-evoked responses (BERs) recorded from a 62-year-old woman with a right frontal glioma, showing a significant increase in the latency of wave V with elevation of lCP. The patient did not show anisocoria.
O'
i
l
,
BER
5.64
5.95
i
lpv
2 msec
that increases in ICP do not necessarily result in prolongation of the latency, especially with the III-V interwave latency. However, for wave V, significantly prolonged latencies were observed in patients with high ICPs over 15 mmHg. At ICPs of -~30 mmHg, the wave V latency approached the upper limit of the normal range or became significantly prolonged. In Figure 2, changes in |CP and BERs are shown in a patient with right frontal glioma. The latency of mass-
m
m
c e Jr-
Figure 3. Serial changes in wave V and III-V interwave latencies before pupillary changes in five patients. Solid and dashed lines indicate "mass side" and "contralateral" auditory brainstem responses, respectively (see text). Thick vertical solid lines indicate the upper limit of wave V and III-V interwave latencies.
side wave V BERs was normal at an ICP of 15 mmHg (left). Three hours later, the ICP increased to 25-30 mmHg, presumably because of respiratory problems, with significant prolongation of the wave V latency (right). The pupils were isocoric and reacted normally to light. Three hours after measurement of BERs, the patient's consciousness deteriorated and the pupils became anisocoric; the diagnosis of early third-nerve stage of uncal herniation was made, as defined by Plum and Posner
15
0 ......
;
mass side
:
c o n t r a l s t e r s l side
D
'5. 0,.
10-
Q
0 X
5
~
$
2 ]]l-V Interwave Latency
"/.
3
~
5
_~*~
~w
~_
6 Wave V Latency
~
,
7 msac
84
Surg Neurol 1987;27:81-6
Nagao et al
Cerebral Infarction
latency in 24 of 27 measurements. However, pupillary normalization was observed on only five occasions (solid circles). Thus, in a large number of the measurements, shortening (normalization) of wave V latencies was observed without clinical improvement of uncal herniation. Less consistent results were indicated in the changes ill I I I - V interwave latencies.
mmHg 110% Glycerol 50
M
Discussion
20, 10. Early IIIrd nerve stage before
1 pv ÷ 0
5
10 msec
Figure 4. Effect of decompression of intracranla/ pressure on the/ateno' of wave V auditory brainstem-evoked responses in a patient with anisocoria due to massive cerebral infarction.
[12]. Thus, a significant change in the latency of wave V preceded the clinical manifestation of uncal herniation in this patient. Sequential changes in the wave V and I I I - V interwave latencies are shown in five patients, whose BERs were measured 3 - 4 8 hours before pupillary changes (Figure 3). On the mass-side BERs, one patient showed abnormal wave V and I ! I - V interwave latencies prior to pupillary changes. In the contralateral BERs, however, four patients exhibited upper limit of normal, or abnormal, wave V latencies 2-15 hours prior to pupillary change. The III-V interwave latencies were abnormal in two patients 4 - 1 0 hours before uncal herniation. Only one patient had normal wave V and III-V interwave latencies for 5 hours in both side BERs before pupillary changes. The effect o f medical decompression of ICP on BERs was illustrated in one patient with anisocoria resulting from massive cerebral infarction (Figure 4). The prolonged latency of wave V (5.98 ms) became normal (5.44 ms) after the ICP decreased from 34 to 16 m m H g with normalization of pupils. Figure 5 summarizes the effects of a decrease in ICP on wave V and I I I - V interwave latencies in patients with uncal herniation manifesting pupillary abnormalities. A decrease in ICP with 10% glycerol solution resulted in shortening of the wave V
In uncal herniation with supratentorial mass lesions, first the rostral midbrain is compressed directly by the herniated brain, and then the dorsal surface of the brainstem, including the inferior colliculus, is displaced caudally more than its ventral surface [6,14]. At the same time, mechanical compression of the upper brainstem causes interference with circulation of the inferior colliculus in the early stage [4]. With this pathophysiological background of uncal herniation, Nagao et al [9,10] reported that changes in the latency and wave form of wave V BERs, which originates predominantly in the inferior colliculus, could indicate early changes of the brainstem function and predict uncal herniation in acute supratentorial expanding lesions. Pupillary change has been shown to be one of the earliest clinical signs of uncal herniation in supratentorial mass lesions. Munro and Sisson [8], however, reported that pupillary changes were not observed in 50% of the patients with uncal herniation verified by autopsy. The main causes for the discrepancy in the clinical manifestation and severity of uncal herniation have been attributed to individual anatomic differences, such as the size and configuration of the tentorial hiatus, the third nerve pathway, the direction of herniated brain, and the displaceable capacity of the brainstem. In these patients, medical or surgical decompression of ICP should be started prior to pupillary changes with the aid of an objective assessment of upper brainstem function. We employed the BERs for this purpose. York et al [ 16] reported a linear relationship between an increase in latency of wave N2 (70 ms) of the visualevoked responses and elevated ICP in patients with hydrocephalus and with cerebral edema. They also showed that, when the N2 latency increased to 90 ms, the ICP increased to a critical level around 400 m m H 2 0 (30 mmHg) [ 15,16]. Significant increases in the latency of wave V BERs and in the central conduction time of the brainstem auditory pathway were indicated in experimentally increased ICP produced by extradural balloon compression [9] and cerebrospinal fluid infusion to the lateral ventricle [7]. Benna et al [2] have documented BER abnormalities consisting of increases in wave I I I - V and I - V latency conduction times and amplitude reductions of wave V in patients with supratentorial tu-
Brainstem Response and Uncal Herniation
Surg Neurol 1987;27:81-6
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Figure 5. Changes in the wave V and I I I - V interwat,e latencies by lowering intracranial pressure (ICP) in patients with uncal herniation. Large solid circles indicate normalization of pupillary abnormality. Decrease in ICP resulted in shortening or normalization of the latency of wave V without significant clinical improvement in most of the trials. Inconsistent changes in the I I I - V interwave latencies were obtained.
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mors who showed clinical signs of increased ICP [2]. However, they did not show the ICP values. Our results show that the latency o f wave V was significantly prolonged even at an ICP o f 20 mmHg. At ICPs o f 30 m m H g , it approaches the upper limit o f the normal value (5.8 ms) or becomes significantly prolonged. Inconsistent latency prolongation occurs in the I I I - V interwave latencies. In head injured patients, Tsubokawa et al [13] showed that prolonged latency or disappearance o f wave V was observed in some cases without brainstem symptoms, and indicated that the BER would provide an early diagnosis of brainstem dysfunction, even when neurological signs are not yet apparent [13]. Ahmed [1] also reported prolongation of I - V interwave latencies in cases of uncal herniation and felt that the changes in the BERs
were noted earlier than clinically seen. In our data with gradual supratentorial expanding lesions, the latency of wave V became abnormal 2 - 1 5 hours before pupillary changes in four of five patients, especially in the "contralateral" BERs. Similar results were reported by Benna et al [2], where four patients had BER abnormalities only on the same side of the tumor, and four patients also showed abnormalities contralaterally. Therefore, it should be emphasized that bilateral measurements of BERs are essential in patients with increased ICP. These facts strongly indicate that in patients with supratentorial mass lesions, the upper brainstem function is critical when ICP approaches 30 mmHg, with significant prolongation o f wave V latency. In this situation, intensive medical or surgical decompression to relieve the ICP should be performed as soon as possible. We have shown
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a reversible change in the latency and amplitude o f wave V in cats that have undergone decompression to alleviate ICP [9]. In our clinical experience, the use o f hypertonic solution to decrease ICP resulted in the shortening or normalization o f the wave V latency in almost all patients with anisocoria. H o w e v e r , pupillary normalization was only observed in 5 o f 27 trials in which decompression was used. In patients without pupillary normalization, or in patients w h o remained clinically unchanged, the effectiveness o f medical decompression o f ICP is obscure, and it is often hard to decide whether or not medical decompression is sufficient for recovery o f brainstem function, and whether or not the same treatment should be continued. Measurement o f wave V BERs seems to provide objective parameters that can be used to assess the effectiveness o f ICP decompression on the brainstem.
The authors gratefully acknowledge the suggestions and revisions of Dr. Robert A. Moody, Chairman of Neurosurgery, Guthrie Clinic, Sayre, Pennsylvania, and Miss Keiko Tanida for preparing the manuscript.
References 1. Ahmed 1. Brain stem auditory evoked potentials in transtentorial herniation. Clin Electroencephalogr 1980;11:34-7. 2. Benna P, Gilli M, Ferrero P, Bergamasco B. Brain stem auditory evoked potentials in supratentorial tumors. Electroencephalogr Clin Neurophysiol 1982;54:8-9. 3. Buchwald JS, Huang C-M. Far-field acoustic response. Origins in the cat. Science 1975;189:382-4. 4. Goodman SJ, Becker DP. Vascular pathology of the brain stem due to experimentally increased intracranial pressure. Changes
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noted in the micro- and macrocirculation. J Neurosurg 1973;39:601-9. 5. Jewett DL. Volume-conducted potentials in response to auditory stimuli as detected by averaging in the cat. Electroencephalogr Clin Neurophysiol 1970;28:609-18. 6. Johnson RT, Yates PD. Brain stem hemorrhage in expanding supratentorial conditions. Acta Radiol (Diagn) 1956;46:250-6. 7. McPherson D, Blanks J, Foltz E. Intracranial pressure effects on auditory evoked responses in the rabbit. Preliminary report. Neurosurgery 1984;14:161-6. 8. Munro D, Sisson WR Jr. Hernia through the incisura of the tentorium cerebelli in connection with craniocerebral trauma. N Engl J Med 1952;247:699-708. 9. Nagao S, Roccaforte P, Moody RA. Acute intracranial hypertension and auditory brain-stem responses. Part i: changes in the auditory brain-stem and somatosensory evoked responses in intracranial hypertension in cats. J Neurosurg 1979;51:669-76. 10. Nagao S, Roccaforte P, Moody RA. Acute intracranial hypertension and auditory brain-stem responses. Part 2: the effects of brain-stem movement on the auditory brain-stem responses due to transtentorial herniation. J Neurosurg 1979;5 l:846-51. l 1. Nagao S, Sunami N, Tsutsui T, Honma Y, Fujimoto S, Ohmoto T, Nishimoto A. Serial observation of brain-stem function in acute intracranial hypertension by auditory brain-stem responses--a clinical study, ln: Ishii S, Nagai H, Brock M, eds. lntracranial pressure. Vol. 5. Berlin, Heidelberg, New York, Tokyo: SpringerVerlag, 1983:474-9. 12. Plum F, Posner JB. The diagnosis of stupor and coma. 3rd ed. Philadelphia: FA Davis, 1980;109-11. 13. Tsubokawa T, Nishimoto H, Yamamoto T, Kitamura M, Katayama Y, Moriyasu N. Assessment of brainstem damage by the auditory brainstem response in acute severe head injury. J Neurol Neurosurg Psychiatry 1980;43:1005-1 l. 14. Weinstein JD, Langfitt TW, Bruno L, Zaren HA, Jackson LF. Experimental study of patterns of brain distortion and ischemia produced by an intracranial mass. J Neurosurg 1968;28:513-21. 15. York DH, Pulliam MW, Rosenfeld JG, Watts C. Relationship between visual evoked potentials and intracranial pressure. J Neurosurg 1981;55:909-16. 16. York D, Legan M, Benner S, Watts C, Further studies with a noninvasive method of intracranial pressure estimation. Neurosurgery 1984;14:456-61.