Acta Oto-Laryngologica

ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20

Selective Resection of the Semicircular Canals of Rabbits with Preservation of Hearing M. Gjuric, M. E. Wigand & W. Hosemann To cite this article: M. Gjuric, M. E. Wigand & W. Hosemann (1992) Selective Resection of the Semicircular Canals of Rabbits with Preservation of Hearing, Acta Oto-Laryngologica, 112:6, 907-915, DOI: 10.3109/00016489209137490 To link to this article: http://dx.doi.org/10.3109/00016489209137490

Published online: 08 Jul 2009.

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Date: 15 March 2016, At: 02:17

Acta Otolaryngol (Stockh) 1992; 112: 907-915

Selective Resection of the Semicircular Canals of Rabbits with Preservation of Hearing M. GJURIC, M. E. WIGAND and W. HOSEMANN From the Department of Otorhinolaryngology, Unwersity of Erlangtn-Nuremberg, Germany

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Gjuric M, Wigand ME, Hosemann W. Selective resection of the semicircular canals of rabbits with preservation of hearing. Acta Otolaryngol (Stockh) 1992; 112: 907-915. The goal of this investigation was to develop a method of surgical removal of the semicircular canals of the rabbit without induction of auditory impairment. Four different surgical techniques were utilized: i) fenestration of the lateral semicircular canal; ii) fibrin glue perfusion of the canal following fenestration; iii) removal of the lateral semicircular canal by drilling after fenestration and fibrin glue perfusion, and iv) removal of all three canals after fenestration and fibrin gluing. Brainstem auditory potentials were recorded repeatedly for up to 3 months after operation and demonstrated preservation of hearing in all rabbits in the first group and in 78% of the second group. In the third group the potentials could be recorded in 67% of the animals and showed a 20 dB deterioration of hearing. After removal of all three semicircular canals residual hearing could be recorded in 50% of the rabbits. These animals regularly showed a 30-40 dB deterioration of hearing. A precise microsurgical technique using fibrin glue and bone chips for interruption of the periand endolymph flow proved crucial for hearing preservation. Key worak: semicircular canals, labyrinth surgery, hearing presetvaiion.

INTRODUCTION Inadvertent surgical injury of the semicircular canals usually results in a complete hearing loss because of the intimate functional relations between the labyrinth and the cochlea (1). On the other hand, slow destruction of the canals by cholesteatoma or temporal bone tumors is not necessarily followed by loss of hearing (2). It is common experience that in some cases of protracted growth of cholesteatoma or tumor and absence of superinfection, cochlear structures may remain untouched in spite of the destruction of the vestibular labyrinth with preserved hearing after partial labyrinthectomy. Precise microsurgical techniques have made the fenestration of the lateral semicircular canal for otosclerosis a safe procedure with only 1-2% incidence of severe hearing loss (3). No report has appeared in the literature concerning intentional surgical separation of the labyrinth from the cochlea with the aim of a functional isolation of the hearing organ. This option, however, would increase the possibilities of functional surgery for tumors and pseudotumors of the internal auditory meatus and the cerebellopontine angle. The intention of this experimental investigation was to develop methods for the safe ablation of the three semicircular canals in a one-stage procedure without induction of a total hearing loss in the affected ear.

MATERIAL A N D METHODS Forty-four adult male rabbits with an average weight of 4 kg were divided into 4 groups. In the first group (4rabbits) the right middle ear was approached through the external ear canal utilizing a retroauricular skin incision. The lateral attic wall and the posterior canal wall were drilled out and the exposed lateral semicircular canal was fenestrated with micro rasps and hooks. The fenestra measured about 2 mm in length and was covered with an overlapping

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Fig. I . Drawings summarizing the operative steps on the semicircular canals of the rabbit. (a) Group 1: Cross-sectionof the fenestrated lateral semicircularcanal ( 1) covered with perichondrium (2); (b)Group 2 Perfusion of the perilymph space (2) of the fenestrated canalwith fibrin glue through a h e needle ( I). Fenestra subsequentlycovered with perichondrium; (c) Group 3 After fibrin glue perfusion the lateral semicircular canal was drilled out with a diamond drill; ( d ) Group 4: Extent of surgical removal of all three semicircular canals preserving the ampullas ( I ) and crus commune (2).

piece of perichondrium (Fig. la). In the second group containing 16 rabbits the fenestration was followed by perfusion of the perilymph space of the lateral semicircular canal with a small amount of fibrin glue using a h e 27 Gauge needle (Fig. Ib). In 11 of these 16 animals the stapes footplate was removed before the transfenestral perfusion of fibrin glue in order to reduce excess pressure. in the labyrinth. The oval window was subsequently closed with connective tissue. In the third group (14 rabbits) the lateral semicircular canal was drilled out after clotting of the injected glue following fenestration and fibrin glue perfusion of the canal (Fig. lc). The openings of the lateral semicircular canal were covered with perichondrium. In the fourth group (10 rabbits) all three semicircular canals were identified by precise drilling and each was “blue-lined‘’ in approximately two-thirds of its length (Fig. Id). Exposure of the entire length of the canals was impossible because of the herniation of the paraflocculus into the temporal bone of the rabbit. The exposure started close to the ampulla and ended on the contralateral side close to the vestibule or crus commune. The perilymph space of the semicircular canals was entered on both exposed ends and the canals were plugged with a small amount of fibrin glue and bone chips preserved during the removal of the ear canal. Subsequently all three canals were removed with a diamond drill. Intramuscular anesthesia with ketamin (50-70mg/kg) and xylazin (4mg/kg) was employed. Brainstem auditory potentials (BERA) were recorded pre- and postoperatively and repeatedly for up to 3 months postoperatively (Fig. 2). A portable BERA audiometer

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Fig. 2. Survey of rabbit groups, postoperative observation time and hearing function. Group I: 1-4; Group 2 (without stapes remmat) 5-9; Group 2 (stapes removaS): 10-20; Group 3 21-34; Group 4 35-44. Black bar: hearing postoperatively preserved. Dotted bar: dead ear. White bar: rabbit succumbed to operation.

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( Westra ERA-Q/S-02, Westra Electronic, W-8901 Welden, Germany) with the click delivered

by means of an Otikon BCX speaker applied to the vertex of the skull was utilized, as previously reported (4). The measurement was started with the stimulus intensity of 60 dB HL, which was then reduced in 10 dB steps. The stimulation by bone conduction was unavoidable because of the surgical approach. The hearing of the non-tested left ear was destroyed several days before the experimental operation on the right ear by simple drilling out of the lateral canal, thus providing the control group. The resulting total deafness of these ears was proven by recording the brainstem responses. The animals were observed for as long as 3 months postoperatively (Fig. 2) and were then killed with an overdose of the anesthetic. The temporal bones were prepared for light microscopic study by the usual technique of perfusion with trialdehyde fixative (5), EDTA decalcification, embedding in paraffin or Spurr’s resin (Polaron Equipment Ltd., Bio-Rad Labs., Watford, UK), serial sectioning and methylene blue or hematoxylin and eosin staining. RESULTS In the control group of rabbits the lateral semicircular canal of the left non-tested ear was destroyed by simple drilling without taking any precautions to preserve the labyrinthine structures. This regularly resulted in complete loss of hearing on the left ear which could be recorded by BERA using the technique of masking the opposite ear as described by Thoma et al. (6) Simple fenestration of the lateral semicircular canal (Group 1) did not cause any significant change of the hearing threshold* throughout the whole postoperative observation period in any of the experimental animals (Fig. 3). Fibrin glue perfusion of the perilymph space of the lateral semicircular canal (Group 2) resulted in preservation of preoperative hearing level in 1 out of the first 4 operated rabbits. Three further rabbits died soon after surgery and could not be included in the study (Fig. 2). The preservation of hearing in 7 of the remaining 9 rabbits (78%) was achieved after removal of the stapes to reduce excess pressure in the labyrinth. The injected fibrin glue caused a mild tissue reaction with granulation tissue formation and was generally resorbed after 4 weeks (Fig. 4). Fourteen rabbits underwent selective ablation of the lateral semicircular canal following the fenestration and fibrin glue perfusion (Group 3). Five animals died in the first postoperative week and were not included in the study ( 1 anesthesia problem, 1 labyrinthitis, 3 rabbits with vertigo and consecutive inanition). Fig. 5 shows the brainstem auditory potentials of rabbit No. 33 with uncomplicated ablation of the lateral canal. Six of 9 controlled rabbits (67%) maintained their hearing postoperatively. They all showed a mild deterioration of the threshold measuring 20 dB throughout the whole postoperative observation period. In the early postoperative period all rabbits showed a characteristic head posture with the operated right ear down and nystagmus to the opposite ear. Histologic evaluation of 3 rabbits with complete postoperative hearing loss showed a large amount of fibrin glue in the vestibule with rupture of the utricle and the saccule which was absent in animals with preserved hearing.

* The authors are aware of the fact that the measurement of the brainstem auditory potentials is not a true measure of hearing but solely provides evidence of neural activity in the auditory system. However, for convenience, the term “hearing” has been used throughout this paper to signify the presence of evoked responses with appropriate auditory stimulation.

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Fig. 3. Auditory evoked brainstem response potentials of rabbit No. 1 (Group I) preoperatively (a) and 3 months after fenestration of the lateral semicircular canal (b) showing no change of the threshold.

Fig. 4. Cross-section of the lateral semicircular canal; 8 weeks after fibrin glue perfusion no trace of the glue can be observed. I endolymphatic canal. 2 perilymph space (rabbit No. 18,

HE, x 80).

After removal of all three semicircular canals (Group 4) the brainstem auditory potentials could be recorded in 5 of 10 rabbits; all displayed a 30-40 dB deterioration of the threshold which remained unchanged in the postoperative follow-up period (Fig. 6). The head posture and nystagmus were identical to what was observed in the previous experimental group and disappeared with time. Histologic examination revealed efficient obliteration of the bony canal stumps with bone chips and connective tissue. Deaf ears showed ruptures of the

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Fig. 5. Auditory evoked brainstem response potentials of rabbit No. 33 (Group 3) before (a) and 3 months after complete removal of the lateral semicircular canal (b). The threshold deteriorated from 20 dB to 40 dB.

membranous labyrinth structures in the vestibule and cochlea and an excess amount of fibrin glue in the animals that died during the first 3 postoperative weeks. In the animals that died later, no fibrin glue remnants could be detected. DISCUSSION Experiments to selectively destroy parts of the vestibular labyrinth date back to 1842 when Flourens demonstrated a resting vestibular function in remnant portions of the labyrinth after partial labyrinthectomy in cats (7). Several other authors have reported that limited mechanical trauma or focal laser irradiation of the single semicircular canal of an experimental animal does not result in degeneration of the organ of Corti when examined by histology or Preyer reflex (8-11). The hearing tests used by these investigators were not very precise, and though they were probably valid in proving the presence of hearing after the operations, the degree of a hearing impairment could not be evaluated. Parnes & McClure performed posterior canal occlusion on 11 guinea pigs and measured the effect on hearing using brainstem evoked audiometry (12). The canal occlusion was obtained by making a small puncture through the posterior semicircular canal with a diamond burr. Eight animals showed no hearing loss while the other 3 had a mild to moderate loss of hearing due to intra-operative complications. The same authors modified their technique by using bone chips for occlusion of the posterior semicircular canal instead of puncture drilling and

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Fig. 6. Auditory evoked brainstem response potentials of rabbit No. 43 (Group 4) before (a) and 3 months after removal of all three semicircular canals (b). The threshold deteriorated from 10dB to

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reported their experiences with 5 patients suffering from intractable benign paroxysmal positional vertigo and with normal hearing (13). Temporary mixed hearing losses occurred in three of the five ears but hearing in all 5 patients ultimately returned to the preoperative level. Kobayashi and colleagues ( 14) have recently reported that during extensive destruction of the lateral semicircular canal of the guinea pig no alteration of the endocochlear potential of the first cochlear turn was Seen and little change in the input-output function curve of the N, component of CAP elicited by 8-kHz tone bursts noted. A similar stability of CAP during destruction of the lateral semicircular canal was recorded in 3 human subjects in the course of translabyrinthine acoustic neuroma surgery. All the above mentioned investigations aimed at finding methods to destroy abnormal vestibular function in Meniere or related disorders. The present investigation, in contrast to the aforementioned, was initiated by the ambition to enhance functional surgery with preservation of auditory function for indications of tumors and pseudotumors of the temporal bone. The technique consisted of a complete surgical removal of the semicircular canals in a one-stage procedure attempting at the separation of both the vestibule and cochlea. To achieve this goal, fibrin glue perfusion of the perilymph space of the fenestrated lateral semicircular canal (Groups 2 and 3) was used to mechanically occlude the peri- and endolymph space (Fig. 7). An excess amount of fibrin glue when entering the vestibule caused disruption of the membranous labyrinth structures which explained the consecutive deafness in 5 animals of the second and in 3 of the third group. The perfusion of the entire length of the canals with fibrin glue when trying to remove all three canals was for this

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Fig. 7. Longitudinal section of

the lateral semicircular canal 2 weeks after fibrin glue perfusion. The fibrin glue causes mechanical occlusion of the membranous endolymphatic canal close to the ampulla. I compressed endolymphatic canal. 2 fibrin glue in the perilymph space. 3 crista ampullaris (rabbit 27, HE, x 80).

reason abandoned and instead the canal ends were plugged with glue and bone chips similarly to the technique of Parnes & McClure. The hearing loss in 5 rabbits was due to violation of the canal endosteum with perilymph leak and damage to the membranous endolymphatic canal very close to the vestibule. This observation is in accordance with the findings of Parnes & McClure (12) and Kobayashi and colleagues (14) who demonstrated that manipulations of the labyrinth closer to the cochlea causes more damage to the hearing. Our animal experiments, though designed to study future applications in clinical otomicrosurgery, cannot be utilized in human patients, at the moment, without further refinement. They have shown, however, that by use of an acute interruption of the perilymphatic and endolymphatic communication between the labyrinthine and cochlear compartments, auditory function can be maintained.

REFERENCES I. Cawthome T. The effect on hearing in man of removal of the membranous lateral semicircular canal. Acta Otolaryngol (Stockh) 1948; Suppl 78: 145-9. 2. Lehnhardt E. Diagnostische und therapeutische Besonderheiten des Felsenbeincholesteatoms. Z Laryngol Rhinol 1967; 46 502- I I. 3. Shambaugh GE. Fenestration operation to otosclerosis. Experimental investigation and clinical observations, in 2 100 operations over a period of ten years. Acta Otolaryngol (Stockh) 1949; Suppl 7 9 1-101. 4. Gjuric M, Wigand ME, Hosemann W, &rg M. Selektive Resektion des lateralen Bogengangs mit GehBrerhaltung-eine tierexperimentelle Studie. HNO 1991; 3 9 476-81. 5. Kalt MR, Tandler B. A study of fixation of early amphibian embryos for electron microscopy. Journal of Ultrastructural Research 1971; 3 6 633-45. 6. Thoma J, Unger U, Kastenbauer E. Funktionelle Auswirkungen des Argon-Lasersam Hororgan des Meerschweinchens. Laryngol Rhinol Otol 1982; 61: 473-6. 7. Flourens JPM. Recherches experimentalessur les propriete et les fonctions du systeme nerveux dans les animaux vertebres. Paris: Bailliere, 1842. 8. Kristensen HK. Acoustic-vestibular and histologic examinations in guinea-pigs after interruption of membranous labyrinth in semicircular canals or cochlea. Acta Otolaryngol (Stockh) 1960; 51: 382-402. 9. Stable J, Hegberg L. Laser and the labyrinth. Acta Otolaryngol (Stockh) 1965; 60: 367-74. 10. Wever EG, Lempert J, Meltzer PE, Rambo JHT. The effects of injury to the lateral semicircular canal. Trans Am Acad Ophthalmol Otolaryngol 1956; 60: 718-27. 11. W i l p k k i C,Stataloff J, Doyle C,Leonard J, Ekhrendt T. Selective vestibular ablation in monkeys by laser irradiation. Laryngoscope 1972; 8 2 1045-58.

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12. Parnes LS, McClure JA. Effect on brainstem auditory evoked responses of posterior semicircular canal occlusion in guinea pigs. J Otolaryngol 1985; 1 4 145-50. 13. Parnes LS, McClure JA. Posterior semicircular canal occlusion in the normal hearing ear. Otolaryngo1 Head Neck Surg 1991; 104: 52-7. 14. Kobayashi T, Shiga N, Hozawa K, Hashimoto S, Takasaka T. Effect on cochlear potentials of lateral semicircular canal destruction. Arch Otolaryngol Head Neck Surg 1991; 117: 1292-5. Manuscript received January 29, 1992; accepted June 12, 1992

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Address for correspondence: Mislav Gjuric, Hals-Nasen-Ohrenklinik, WaldstraDe 1, W-8520 Erlangen, Germany

Selective resection of the semicircular canals of rabbits with preservation of hearing.

The goal of this investigation was to develop a method of surgical removal of the semicircular canals of the rabbit without induction of auditory impa...
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