Effects of cerebellar retractions on the cochlear nerve - Springer Link

:Acta N6urochirurgica

Acta Neurochir (Wien) (1988) 90:45-52

9 by Springer-Verlag1988

Effects of Cerebellar Retractions on the Cochlear Nerve: an Experimental Study on Rhesus Monkeys T. Sekiya * and A. R. M~ller Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, U.S.A.

Summary

itoring b r a i n s t e m a u d i t o r y evoked potentials (BAEP)

Cerebellar retractions were performed in the cerebellopontine (CP) angle of rhesus monkeys to study the relationship between changes in brainstem auditory evoked potentials (BAEP) and/or compound action potentials (CAP) from the cochlear nerve, and morphological changes in the cochlear nerve in order to investigate the nature of cochlear nerve injuries caused by this surgical procedure. The changes in the BAEP and/or CAP from the cochlear nerve that were seen during cerebellar retraction were similar to those seen in human patients during operation. After completion of each experiment the temporal bones were prepared for histological examination. Hemorrhages often developed at the fundus of the internal auditory canal as a direct result of cerebellar retraction. These hemorrhages were located at the area cribrosa, where the branches of the internal auditory artery penetrate the cribriform plate. As the hemorrhages appeared to be due to avulsion rupture of these branches, they were considered to be the probable cause of the sudden loss of all the components of the auditory responses. The cochlear nerve fibers, especiallythose at the basal turn of the cochlea, avulsed simultaneously at the area cribrosa in most cases.

a n d c o m p o u n d action potentials (CAP) recorded directly from the eighth nerve has reduced these risks to some extent 5, 13 15, 2J. However, it is n o t k n o w n how

Keywords: Area cribrosa; brainstem auditory evoked potentials; cerebellopontineangle;cochlear nerve; hearing preservation; internal auditory artery; cerebellar retraction. Introduction The cochlear nerve is frequently exposed d u r i n g neurosurgical procedures, such as in operations to remove cerebellopontine (CP) angle t u m o r s 8, 15, 18, arterioven o u s m a l f o r m a t i o n s 2, a n d for microvascular dec o m p r e s s i o n of cranial nerves 7, 9. The cochlear nerve is k n o w n to be v u l n e r a b l e to surgical m a n i p u l a t i o n s , a n d hearing is often i m p a i r e d or lost in o p e r a t i o n s in which the eighth nerve has been exposed. The exact cause of cochlear nerve injuries is n o t k n o w n in detail, a n d how these injuries result from CP angle m a n i p u lations is n o t fully u n d e r s t o o d . Nevertheless, the recent i n t r o d u c t i o n of electrophysiological m e t h o d s for mort-

changes in the recorded potentials are related to morphological changes in the a u d i t o r y nerve, n o r is it k n o w n exactly which kinds of m o r p h o l o g i c a l changes result from m a n i p u l a t i o n s in the CP angle. The aim of the study described in this report was to correlate changes in a u d i t o r y evoked potentials that occur as a result of cerebellar retraction with the morphological changes in the cochlear nerve of a n a n i m a l in which the relationship between the cerebellum a n d the eighth nerve has a close a n a t o m i c a l similarity to that of m a n . By such correlations we hope to gain a better u n d e r s t a n d i n g of the m e c h a n i s m s involved in such injuries to the cochlear nerve.

Materials and Methods Sixteen adult rhesus monkeys, each weighing 3.5 to 5 kg, were used in this study. The animals were obtained from laboratories performing chronic studies on these animals, when they were to be sacrificed becausethey were no longer of use for these chronic studies. In several of the animals other experiments had been performed previous to the study of the auditory system. Each animal was initially anesthetized with Ketamine HC1 8 mg/ kg and pentobarbital sodium (Nembutal| 12.5 mg/kg bodyweight, administered intramuscularly: Fentanyl citrate and Droperidol (Innovar-Vet| 0.25 ml/kg bodyweight was intermittently injected intramuscularly during the experiment. Respirations were controlled with a small animal respirator, cardiac function was monitored electrocardiographically, and rectal temperature was kept between 36 and 38 ~ with the aid of a heating pad. The cerebellum was retracted medially to expose the internal auditory meatus. In the rhesus monkey (as in man) the parafloccular portion of the cerebellumis in contact with the dorsal surface of the seventh and eighth cranial nerves, and may extend into the internal auditory canal. Thus the paraflocculus was first removed to permit

46

T. Sekiya and A. R. Moller: Effects of Cerebellar Retractions on the Cochlear Nerve

inspection of the nerves at the internal auditory meatus, and then the lateral edge of the cerebellum was retracted medially. This retraction of the cerebellum applied traction force to the cochlear nerve. All manipulations were done in a manner similar to the way in which the human cerebellum is retracted during an operation in which a retromastoid craniectomy is performed to gain access to the CP angle, and BAEP were recorded continuously during the experiment. BAEPs were recorded throughout the experiments by needle electrodes placed on the vertex, with the reference electrodes placed on the back of the neck and a ground electrode placed at the base of the tail. A Teflon-coated wire (Medwire *, Type AG10T), with about 0.2 mm bared at its tip, was used to record compound action potentials (CAP) directly from the auditory nerve or in its vicinity after the nerve had been sufficiently exposed. Needle electrodes (Grass Instrument Co. **, Type E2 subdermal) were used to record from other sites. Click stimuli were presented to the right ear (operative side) at a rate of 10 pps through miniature stereo earphones (Radio Shack ***, Realistic) driven by a 30-V, 20-gsec rectangular pulse wave fed by a stimulator (Grass Instrument Co. **, Type SD9). The peak sound pressure was 1I5 dB SPL, measured in a 1-cc acoustically damped cavity. The recorded potehtials were amplified with a bandpass of 3 Hz to 10 kHz and averaged using an LSI 11/73 processor at a sampling interval of 30 gsec with 256 datapoints in each recording. The averaged responsed were then filtered digitally. Digital filtering does not displace the peaks but enhances them and suppresses noise 12 Postoperatively, each animal was perfused transaortically with 4% paraformaldehyde, 0.5% glutaraldehyde, and 0.56% dextrose in a 0.1 M phosphate buffer (pH 7.2 to 7.4). This perfusion method cleared the red blood cells from the entire cochlea and cochlear nerve on the control side. Simultaneously, the eighth nerve was irrigated in situ with the same fixatives through a catheter placed in the CP angle on the operative side. Two hours later both temporal bones and the brainstem were taken out en bloc, using the utmost caution not to move CP angle structures, and were then immersed in the same fixatives for 2 days at 4 ~ After 2 days both temporal bones were removed and decalcified with EDTA and NaOH solution 22. Serial thick sections were cut and stained with toluidine blue solution and examined under a light microscope. The non-operated side of each animal served as the control for the operated side. When the non-operated side contained unacceptable artifacts, all the results from that animal were rejected.

tencies of the NI and N2 peaks in the CAP recorded from the auditory nerve which occurs immediately after the retraction. There is often a brief increase in the amplitudes of these two negative peaks, as illustrated in Fig. 1 a (16:56), followed by a progressive decrease in the amplitude of the CAP components. The decrease in the amplitude of the CAP components persisted after the retraction had been released, as is illustrated in Fig. 1 a. Two hours and fifty minutes after retraction (19 : 08), in the animal that is illustrated in Fig. 1 a, the waveform of the CAP appeared to be stable and the perfusion was begun at that time. As shown in Fig. 1 b and c, there were significant changes at the area cribrosa; hemorrhages had occurred and some of the foramina at the area cribrosa that normally contain bundles of cochlear nerve fibers were empty. The cochlear nerve fibers of the basal portion of the cochlea were markedly stretched and seemed to lose their continuity. Similar changes in the CAP did not always mean similar histological findings. In the experiment illustrated in Fig. 2 from another monkey there was a depression of the N1 and N2 components similar to that shown in Fig. 1 a (Fig. 2 a). However, the cochlear nerve in this animal remained morphologically intact, as viewed under the light microscope: there were no

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The results shown in Fig. 1 a reveal the typical changes in the compound action potentials (CAP) from the auditory nerve seen in eleven of the monkeys as a result of cerebellar retraction. In these monkeys the cerebellar edge was intentionally retracted after the parafloccular portion of the cerebellum was dissected. Such a retraction results in a prolongation of the la-

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Fig. 1 a. Serial recording of the compound action potentials (CAP). Cerebellar retraction (CR) caused transient increments of NI and N 2 amplitudes (16: 56), but two hours and fifty minutes after the retraction, the amplitudes of N] and N2 components significantly decreased (19:08)


47

Fig. 1 b. Thick arrows indicate hemorrhages at the area cribrosa, while hemorrhages are also identifiable around the branches of the internal auditory artery. The cochlear nerve fibers of the basal portion of the cochlea are markedly stretched (thin arrows). CO cochlear nerve

Fig. 1c. Enlarged view of the area cribrosa indicated by the bar in Fig. 1b. Hemorrhages (h) at the area cribrosa. Arrows indicate empty foramina due to avulsion of the cochlear nerve fibers. On the other hand, some cochlear nerve fibers still remained continuous across the cribriform plate (arrowheads), sgc spiral ganglion cells in the canalis spiralis modioli

significant h e m o r r h a g e s in the a r e a c r i b r o s a a n d there were no signs o f cochlear nerve avulsion. T h e m o r e p r o x i m a l p o r t i o n o f the cochlear nerve also seemed to be intact (Fig. 2 b). A m o n g the eleven a n i m a l s with similar changes in the e v o k e d potentials, four did n o t show a n y m o r p h o l o g i c a l changes when e x a m i n e d with light m i c r o s c o p y . In four animals, the C A P f r o m the a u d i t o r y nerve were s u d d e n l y lost d u r i n g cerebellar retraction. In one o f these a n i m a l s the negative p e a k s o f the C A P were

s u d d e n l y lost when the r e t r a c t o r was a d v a n c e d to retract the deep p a r t o f the cerebellum (Fig. 3 a). T h e histological e x a m i n a t i o n o f this a n i m a l disclosed hemo r r h a g e s at the a r e a c r i b r o s a (Fig. 3 b), with some hemo r r h a g e extending into the spiral g a n g l i o n p o r t i o n o f the b a s a l t u r n o f the cochlea (Fig. 3 c). I n the o t h e r three animals, h e m o r r h a g e s were f o u n d a b u t t e d to the a r e a c r i b r o s a as in Fig. 3 b. Fig. 4 a shows changes in the B A E P d u r i n g retraction o f the cerebellum (seen in only one o f the eleven

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Fig. 2 a. Serial recordings of the CAP. Cerebellar retraction depressed N~ and N2. Compare with Fig. 1 a

Fig. 2 b. At the area cribrosa no hemorrhagic focus was identified and the cochlear nerve fibers did not avulse (small black arrows). White arrows indicate well-preserved Schwann-glial junctions. Thick black arrow indicates the spiral ganglion cells in the canalis spiralis modioli

animals). A f t e r the cerebellar retractions only wave o f the B A E P r e m a i n e d (Fig. 4 a). I n this case, no hemo r r h a g e s were identified at the a r e a cribrosa, a n d the cochlear nerve fibers also seemed to m a i n t a i n their c o n t i n u i t y (Fig. 4 b).

Discussion The results o f the present study show t h a t retraction o f the cerebellum m a y cause injury to the c o c h l e a r nerve n e a r the a r e a c r i b r o s a a n d avulsion r u p t u r e o f the internal a u d i t o r y artery.

The internal a u d i t o r y artery is the only artery t h a t supplies the cochlea a n d the cochlear nerve a n d its s u r r o u n d i n g structures 3, 16. The internal a u d i t o r y artery ramifies into three m a j o r b r a n c h e s within the internal a u d i t o r y c a n a l - - t h e cochlear artery, the vestib u l o c o c h l e a r artery, a n d the a n t e r i o r vestibular art e r y - a n d p e n e t r a t e s the c r i b r i f o r m plate t h r o u g h b o n y f o r a m i n a at the b o t t o m o f the internal a u d i t o r y canal 3, 16. The internal a u d i t o r y a r t e r y also sends n u m e r o u s branches to the s u r r o u n d i n g structures, such as the p e r i o s t e u m within the internal a u d i t o r y canal 16. The


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Fig. 3 a. Serial recordings of the CAP. During the cerebellar retraction (CR), all the components of the CAP were suddenly lost (14 : 43)

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Fig. 3 b. Hemorrhages (h) are indicated by thick black arrows at the area cribrosa (white hollow arrows). Cochlear nerve fibers entering the modiolus are compressed by hemorrhages (white arrowheads). Thin black arrows indicate the cochlear nerve fiber bundles in the modiolus, sgc spiral ganglion cells in the canalis spiralis modioli

branches of the internal auditory artery that penetrate the cribriform plate in man are all less than 100 gm in diameter 6, 16. Our study indicates that these branches of the internal auditory artery are prone to avulse with surgical manipulation, and that avulsion of the cochlear nerve fibers, especially at the basal turn of the cochlea, occurred simultaneously at the area cribrosa. It is often reported that BAEP are suddenly lost during operations in the CP angle, and that these events

are followed by postoperative hearing loss that may be profound. Raudzens and Shetter 17 have reported such complications in operations in which cerebellar retraction was deepened to the trigeminal nerve root during a microvascular decompression procedure, and Ojeman et al. 15 reported that the BAEP were suddenly lost during internal decompression of acoustic neuromas. Abramson et al. 1 reported that BAEP were irreversibly lost in acoustic tumor operations during

50

T. Sekiya and A. R. Moiler: Effects of Cerebellar Retractions on the Cochlear Nerve

Fig. 3 c. Hemorrhages (h) extend to spiral ganglioncells(sgc) in the basal turn of the cochlea. Arrows indicate proximal processes of the bipolar neurons

drilling of the internal auditory canal and manipulation of the cochlear nerve to complete the removal of the tumor. Histological evaluation of animals in .our study in which there was a similar sudden extinction of auditory evoked potentials (BAEP or CAP) uniformly showed massive hemorrhages at the area cribrosa, indicating that rupture of the branches of the internal auditory artery had occurred at the area cribrosa. Thus, it seems reasonable to assume that the sudden loss of BAEP during CP angle operations may be caused by avulsion rupture of the internal auditory artery at the area cribrosa. Vasospasm of the internal auditory artery has been propounded as a cause for the loss of cochlear function during CP angle operations 19, 20. Recently, it was reported that oculomotor nerve palsy could occur due to cerebral vasospasm 10, but such a report is not available on the cochlear nerve. Thus, it still remains to be clarified whether vasospasm of the internal auditory artery can be a cause of loss of auditory function in operations at the CP angle. We show in the present study that the BAEP can change in such a way that only wave I is preserved while the other components of the BAEP are lost (Fig. 4 a). Since histological study of the animal shown in Fig. 4 a failed to identify any sign of rupture of the internal auditory artery, the blood supply to the cochlea was considered to be essentially intact; this supports

the assumption that if peak I is preserved the cochlea and at least the distal portion of the auditory nerve are functioning. It seems more likely that mechanical stress from CP angle manipulations in this animal had injured the cochlear nerves where they pass through the area cribrosa, thus causing a nerve conduction block in the portion of the nerve that is proximal to the generator site of wave I of the BAEP (extracranial portion of the cochlear nerve). Levine et al. 11 reported seeing similar changes clinically; they noted loss of wave II and the following components during removal of an acoustic neuroma, so that only wave I was left intact in the acute postoperative period. Grundy et al. 5 described an operation to perform microvascular decompression of the facial nerve to relieve hemifacial spasm in which all other components but peak I were temporarily obliterated. In four of the animals in which the CAP was not distinguishable after retraction, it could not be ruled out that some auditory nerve fibers were not pulled out. It is thus inherently difficult to determine the morphological basis for electrophysiological conduction block of nerve impulses with light microscopy, except in the case of definite disruption of the cochlear nerve fibers at the area cribrosa. This may explain why abnormal BAEP findings appear without light microscopic manifestation of cochlear nerve injury. The relationship between intraoperative BAEP changes and postoperative psychoacoustic hearing level

T. Sekiya and A. R. Moiler: Effects of Cerebellar Retractions on the Cochlear Nerve

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is uncertain 4, 15 and the preservation of auditory evoked potentials during operations in the CP angle does not necessarily equate with useful postoperative hearing 15. However, most clinical reports admit that abrupt and irreversible loss of BAEP indicates a p o o r prognosis for postoperative preservation of useful hearing 1,15, 17. The results of the present study indicate that the underlying mechanism responsible for this type of intraoperative change in the BAEP m a y be avulsion rupture of the internal auditory artery. It has been clinically known that anatomical preservations of the cochlear nerve does not always mean preservation of function. This may be due to the fact that morphological changes of the cochlear nerve due to manipulations in the CP angle occur at the most distal portion of the internal auditory canal which is not exposed. The fragility of the cochlear nerve has been generally attributed to the fact that the CP angle portion of the cochlear nerve is covered by central myelin, and it is thus assumed to be more susceptible to mechanical manipulation than nerves covered with peripheral myelin. In our study, however, conduction block in the cochlear nerve was caused by cerebellar retractions even when not directly manipulating the cochlear nerve, and there were no verifiable morphological changes in the proximal portion of the cochlear nerve trunk. Therefore, avulsions of cochlear nerve fibers and the internal auditory artery at the area cribrosa should be regarded as an additional explanation

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of the fragility of the cochlear nerve besides the inherent fragility of the intracranial portion

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Acknowledgements This study was supported in part by a grant from the National Institutes of Health (to Dr. A. R. Moller, No. 1 R01 NS 21378-02). We thank Dr. Peter J. Jannetta for making the resources of the Department of Neurological Surgery available to us. The help of Dr. Raymond Lund, Professor and Chairman, Department of Anatomy and Cell Biology, and Dr. A. Julio Martinez, Professor, Department of Pathology (Neuropathology), University of Pittsburgh School of Medicine, is greatly appreciated. We express our thanks to Mr. James ApicelIa, Department of Anatomy and Cell Biology, and Ms. Victoria Elliott for technical assistance, and Ms. Diana Mathis and Ms. Cleat Szczepaniak for editorial assistance.

References 1. Abramson M, Stein BM, Emerson RG, Pedley TA, Wazen JJ (1985) Intraoperative BAER monitoring and hearing preservation in the treatment of acoustic neuromas. Laryngoscope 95: 1318-1322 2. Drake CG, Friedman AH, Peerless SJ (1986) Posterior fossa arteriovenous malformations. J Neurosurg 64:1-10 3. Fisch U (1968) The surgical anatomy of the so-called internal auditory artery. In: Hamberger CA, Wersall J (eds) Proceedings of the Tenth Nobel Symposium. Almqvist and Wiksell, Stockholm, pp 121-130 4. Fria TJ (1985) Threshold estimation with early latency auditory potentials. In: Katz J (ed) Handbook of clinical audiology, edn 3. Williams and Wilkins, Baltimore, pp 549-564 5. Grundy BL, Lina A, Procopio PT, Jannetta PJ (1981) Reversible evoked potential changes with retraction of the eighth cranial nerve. Anesth Analg 60:835-838 6. Ishii T (1966) Arteries from basal brain to inner ear. Observation of 20 Japanese. J Otorhinolaryngol Soc Jpn 67:1387-1399 (English abstr) 7. Jannetta PJ (1982) Cranial rhizopathy. In: Youmans JR (ed) Neurological Surgery, edn 2, vol 6. WB Saunders Co, Philadelphia, pp 3771-3784 8. Jannetta PJ, Moller AR, Moller MB (1984) Technique of hearing preservation in small acoustic neuromas. Ann Surg 200: 513523

9. Jannetta PJ, Moiler MB, Moiler AR (1984) Disabling positional vertigo. New Eng J Med 310:1700-1705 10. Kudo T (1986) Postoperative oculomotor palsy due to vasospasm in a patient with a ruptured internal carotid artery aneurysm: A case report. Neurosurgery 19:274-277 1i. Levine RA, Montgomery WW, Ojemann RG, McGaffigan PM (1984) Monitoring auditory evoked potentials during acoustic neuroma surgery. Insights into the mechanism of hearing loss. Ann Otol Rhinol Laryngol 93:116-123 12. Moiler AR (1983) Improving brainstem auditory evoked potential recordings by digital filtering. Ear Hear 4:103-113 13. Moiler AR, Jannetta PJ (1983) Monitoring auditory functions during cranial nerve microvascular decompression operations by direct recording from the eighth nerve. J Neurosurg 59: 493499 i4. Moller MB, Moiler AR (1985) Loss of auditory function in microvascular decompression for hemifacial spasm. Results of 143 consecutive cases. J Neurosurg 63:17-20 15. Ojemann RG, Levine RA, Montgomery WM, McGaffigan PM (1984) Use of intraoperative auditory evoked potentials to preserve hearing in unilateral acoustic neuroma removal. J Neurosurg 61:938-948 16. Portmann M, Sterkers JM, Charachon R, Chonard CH (1975) The Internal Auditory Meatus. Anatomy, Pathology and Surgery. Churchill-Livingstone, London, pp 35 52 17. Raudzens PA, Shetter AG (1982) Intraoperative monitoring of brain-stem auditory evoked potentials. J Neurosurg 57:341 348 18. Samii M (1985) Microsurgery of acoustic neurinomas with special emphasis on preservation of seventh and eighth cranial nerves and the scope of facial nerve grafting. In: Rand RW (ed) Microsurgery. CV Mosby Co, St. Louis, pp 366-388 19. Sekiya T, Iwabuchi T, Andoh A, Kamata S (1983) Changes of the auditory system after cerebellopontine angle manipulations. Neurosurgery 12:80 85 20. Sekiya T, Iwabuchi T, Kamata S, Ishida T (1985) Deterioration of auditory evoked potentials during cerebellopontine angle manipulations. An interpretation based on an experimental model in dogs. J Neurosurg 63:598-607 21. Silverstein H, Norrell H, Hyman S (1984) Simultaneous use of CO2 laser with continuous monitoring of eighth cranial nerve action potential during acoustic neuroma surgery. Otolaryngol Head Neck Surg 92:80-84 22. Warshawsky H, Moore G (1967) A technique for the fixation and decalcification of rat incisors for electron microscopy. J Histochem Cytochem 15:542-549 Authors' address: Department of Neurosurgery, Hirosaki University, 5 Zaifu-cho, Hirosaki-shi, Aomori-ken, 036 Japan.