The Journal of Laryngology and Otology October 1979. Vol. 93. pp. 955-968
The effects of vascular occlusion on the human inner ear By A. BELAL, Jr., M.D.* (Los Angeles, California) DISORDERS of microcirculation, which are well documented in areas other than the inner ear, might be expected to develop in the inner ear despite the lack of documentation. Von Fieandt and Saxen (1937) described two types of inner ear pathology in old age: senile atrophy of the spiral ganglion and angiosclerotic degeneration of the inner ear. The latter condition is marked by thickening of strial and other cochlear vessels and loss of capillaries followed by sensorineural degeneration. Jorgensen (1961) described a close relationship between cochlear angiopathy and atherosclerosis of the blood vessels in the base of the skull, as well as generalized atherosclerosis. Schuknecht (1964) was the first to draw attention to the effect of strial atrophy on hearing thresholds. Johnsson (1973), who used the surface preparation technique to study human cochlear blood vessels, found that strial atrophy was a common denominator in sensorineural hearing loss. It is tempting for the clinician to assume that many inner ear disorders are caused by vascular pathology affecting the blood supply to the ear. This assumption is the basis of treatment for Meniere's disease, sudden deafness, tinnitus, and other conditions. A vasodilator regimen of intravenous histamine, sublingual and intramuscular histamine, nicotinic acid, probanthine, and benadryl may be prescribed (Sheehy, 1975), or sympathectomy may be performed (Passe, 1953; Johnsson, 1954; GoldingWood, 1969). However, the otologist must remember that histological evidence of vascular pathology in these conditions remains almost completely lacking. This paper is the first review of the effects of depriving the human inner ear of its blood supply. The temporal bones of two patients who had undergone middle fossa surgery—one for vestibular nerve section in Meniere's diseaseand onefor removal of an acoustic tumour—during which the blood supply to the inner ear was deliberately cut, were studied. Both sets of bones have been recently reported (Belal et ah, 1979 a and b respectively). Findings are correlated with the vascular pathology of inner ear problems.
Arterial blood supply of the inner ear
It is generally agreed that only one vessel, the internal auditory artery, supplies the human inner ear. Although there are great variations in the * Research Fellow (1978-1979), Ear Research Institute, Los Angeles, California, and Assistant Professor of Otolaryngology, Alexandria Medical School, Alexandria, Egypt. 955
956
A. BELAL
origin, size, length, course, and ramification of this vessel (Mazzoni, 1970), it divides characteristically into the common cochlear artery and the anterior vestibular artery. The common cochlear artery divides into the main cochlear and vestibulocochlear branches. The latter divides into the posterior vestibular artery and the cochlear ramus (Fig. 1). The usual distribution of these vessels is as follows: The main cochlear artery supplies three-fourths of the cochlea, while the cochlear ramus supplies the basal one-fourth. The anterior vestibular artery supplies the superior surfaces of the utricle, saccule, and superior and lateral semicircular canals. The posterior vestibular artery supplies the posterior semicircular canal and the inferior surfaces of the utricle and saccule. Venous drainage of the inner ear
The venous drainage of the inner ear has been described in detail by Schuknecht (1974). The main veins of the cochlea are the posterior and anterior spiral veins. The posterior vein drains the scala media (external wall), scala vestibuli and spiral ganglia. The anterior vein drains the spiral lamina and scala tympani. These two veins join near the base of the
Wear Duct
FIG. 1 Diagram of the arterial blood supply of the inner ear.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR
957
cochlea to form the common modiolar vein. This is joined in turn by the vestibulocochlear vein to become the vein at the cochlear aqueduct. This main venous channel runs along the cochlear aqueduct to empty into the inferior petrosal sinus. The vestibular labyrinth is drained by the anterior and posterior vestibular veins. These veins join the vein of the round window to become the vestibulocochlear vein. In addition, the semicircular canals are drained by veins that form the vein of the vestibular aqueduct. This accompanies the endolymphatic duct and drains into the lateral sinus. Effect of anterior vestibular artery occlusion
Silverstein and Makimoto (1973), in two sets of experiments on cats, sectioned the superior vestibular and singular nerves and their accompanying vessels in one experiment and only the nerves in the other. Severe degenerative changes in the vestibular labyrinth occurred only in the first instance. Lindsay and Hemenway (1956) described a syndrome of sudden onset of severe vertigo without deafness that gradually resolved in a matter of weeks. This was followed by positional vertigo persisting for weeks or years. The authors suspected the syndrome to be due to occlusion of the anterior vestibular artery. Our study of the previously cited temporal bone (Belal et al., 1979a) found severe degeneration of the utricular and saccular maculae and the cristae of the lateral and superior semicircular canals (Fig. 2). Both canals were filled with fibrous and osteoid tissue. The rest of the membranous labyrinth looked normal (Fig. 3). Figure 4 depicts the effects of blockage of the anterior vestibular artery on the human inner ear. Effect of internal auditory artery occlusion
Perlman et al. (1959) showed that occlusion of the internal auditory artery in guinea-pigs for five minutes produced spotty, degenerative changes in the cochlea, principally in the hair cells and spiral ganglia. Damage to hair cells was severe in the basal turn of the cochlea. Permanent obstruction of the arterial blood supply caused disintegration of the cochlea to begin immediately, with complete necrosis occurring within 24 hours. Progressive fibrosis and ossification of the cochlear spaces followed. The effects of internal auditory artery occlusion on the human ear were illustrated in the previously cited temporal bone (Belal et al., 1979b). Because the internal auditory artery was sacrificed during surgery, the patient completely lost his hearing. Histopathological examination showed severe degenerative changes and ossification of the cochlea and the entire vestibular labyrinth (Fig. 5). Cochlear ossification was pronounced in the basal and middle turns. In addition, ossification involved only the scala tympani (Fig. 6). All turns of the scala vestibuli were free of new bone
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A. BELAL
Fto. 2 The superior vestibular nerve and the anterior section. nerve r vestibula Right middle fossa t e the m a r k Servin to d n a l ery superior v e s S * ™ " t hise denervat ^ '*£The "*'• ^ f nerve. ormath nefve"r ed and new bone formation appears in the utricle the ffac.al nerve from lateral semicircular canal.
u^gTiv.-Inferio r V&rjtii>u\ii • - < ' Nerve FIG. 3 r and singular nerves were cut. The saccule is vestibula inferior Same case as in Fig. 2. The ng of Reissner's denervated and collapsed. The cochlea looks normal except for the ballooni membrane in the apical coil.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR
959
ochlear Duct
FIG. 4 Diagram of the effects of anterior vestibular artery occlusion on the human inner ear.
formation. Ossification and degeneration pervaded the vestibular labyrinth except for the endolymphatic duct and sac, which appeared normal (Fig. 7). The pattern of cochlear ossification after arterial blood supply deprivation seems to be related to the anatomy of venous drainage of the cochlea. Smith (1954) has shown that the radiating arterioles supplying the cochlea arise at regular intervals from the common cochlear artery. These arterioles pass over the scala vestibuli and scala media to form capillaries, which are drained by collecting venules in the lower part of the spiral ligament. Thus, the main venous drainage crosses over the scala tympani. The cochlear venous channels run caudalward from apex to base to drain into the vein of the cochlear aqueduct. Ossification presumably occurs due to haemorrhage in the perilymphatic spaces. Haemorrhage starts in cochlear areas with good access to venous nonoxygenated blood. This substantiates the theory that labyrinthine ossification occurs from perivascular or adventitial cells around capillaries (Paparella and Sugiura, 1967). These undifferentiated mesenchymal cells give origin to osteoblasts that induce new bone formation. The possibility of arteriolar anastomosis between the middle ear
960
A. BELAL
Remnant of Acoustic Neuroma
Ossified Vestibule Ossified Lateral 'Degenerated Cochtear Nerve
FIG. 5 Right middle fossa removal of acoustic tumour. The internal auditory artery was cut during the operation. Degeneration and ossification cover the entire inner ear except for the apical coils of the cochlea and ths endolymphatic duct and sac. The cochlear nerve has degenerated, and a remnant of the tumour remains in the antero-inferior compartment of the internal auditory canal.
Degenerated Organ Of Cortr
FIG. 6 Same case as in Fig. 5. The basal coil of the cochlea shows new bone formation in the scala tympani, modiolus and spiral ligament. The sensorineural structures have completely degenerated.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR
Posteri o r Fossa FIG. 7 Same case as in Fig. 5. Endolymphatic duct and sac are normal.
Endotymphatic-p
^ ^Anastomoses ?
hlear Duct
FIG. 8 Diagram of the effects of internal auditory artery occlusion on the human inner ear.
961
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A. BELAL
in promontory, otic capsule and apical half of the cochlea should be kept area,' key lar 'Vascu the as mind. Hansen (1971) described this anastomosis the a highly vascularized area of endochondral bone situated between canal y auditor l interna and cochlea, vestibule, middle ear, promontory sac fundus. The normal appearance of the endolymphatic duct and the of dura the from supply blood suggests the presence of a collateral rative degene of ution distrib the shows 8 posterior cranial fossa. Figure changes in the inner ear after internal auditory artery occlusion. Effect of arterial and venous occlusion on the cochlea
Perlman and Kimura (1957), obstructing the venous drainage in animal studies, found that degeneration of the outer hair cells was evident within 24 hours and the number of ganglion cells was reduced within two weeks. first The stria vascularis was particularly susceptible, often showing the days seven to up seen signs of damage. Haemorrhages were commonly ve after obstruction. Subsequent fibrosis and ossification were less extensi tion. obstruc with venous obstruction than with arterial Effects of occlusion of the arterial blood supply and of venous drainage of the cochlea were seen in the temporal bones of five patients who underwent a translabyrinthine removal of cerebellopontine angle tumours. With the this surgery, both the arterial blood supply and the venous drainage of
Facial Nerve
i 9 . The arterial supply and venous drainage neuroma acoustic of Left translabyrinthine removal sclerosis is total. of the cochlea were presumably cut in the course of surgery. Cochlear FIG.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR
963
cochlea are cut. The temporal bones showed total osseus sclerosis of the cochlea (Fig. 9). Ossification involved all the scalae of the cochlear duct and all the cochlear turns were similarly ossified (Fig. 10). Thus, it seems that occlusion of both arterial and venous blood channels results in more severe degeneration and sclerosis of the cochlea than arterial occlusion alone. Ischemic changes presumably occur early, so that anastomotic channels do not have sufficient time to develop. Probable vascular etiology of inner ear diseases
Histopathological changes that have been described should be evaluated critically. Vascular effects could be secondary to the primary pathology in the inner ear or to the surgical procedure undertaken to treat it. However, histopathological studies did not focus on the microvascular network of the inner ear because it is not clearly seen in conventional celloidin sections. Given this limitation, the observations presented suggest important implications for vascular diseases of the inner ear and their treatment. The most common of these diseases is sudden sensorineural hearing impairment. The two most popular concepts to explain this condition are viral labyrinthitis (Schuknecht et al., 1973) and vascular occlusion (Fowler, 1950; Hilger and Goltz, 1951; Sheehy, 1960). To date, all pathological
FIG. 10 Same case as in Fig. 9. Bone totally obliterates the apical and middle turns of the cochlea.
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material from temporal bones of patients with this disease shows a situation different from what we have described. The most consistent pathological change in these bones is atrophy of the organ of Corti. No temporal bones have shown fibrous or bony proliferation in the inner ear. Although vascular conditions, such as leukaemia, Buerger's disease and macroglobulinaemia, can produce sudden hearing loss, most cases are due to viral, rather than vascular, etiology. Thus, a vasodilator regimen seems unlikely to have value in the treatment of most of these cases. The similarity of the pattern of cochlear sclerosis associated with labyrinthitis ossificans and that associated with deprivation of blood supply (Fig. 11) seems to be more than coincidental. Labyrinthitis ossificans is the healed stage following labyrinthitis, whether otic or meningitic in origin. New bone formation in these cases seems to be due to deprivation of the blood supply to the membranous labyrinth. Septic embolization, followed by haemorrhages in the perilymphatic spaces, is a probable explanation for the pathogenesis of new bone in the labyrinth. Atrophy of the stria vascularis is a common cause of hearing loss that is bilateral and symmetrical, with flat audiometric patterns and excellent speech discrimination (Schuknecht et al., 1974). The temporal bones of persons with this type of hearing loss show atrophic changes in the stria vascularis, most of which are localized in the apical regions of the cochlea
FIG. 11 Labyrinthitis ossificans. There is total osseous sclerosis of the cochlea. The labyrinthine spaces and modiolus have been replaced by lamellar bone. The borders of the new bone can be readily distinguished from the surrounding otic capsule.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR 965
(Fig. 12). The resemblance between these findings and those following venous obstruction (Kimura and Perlman, 1956) suggests the possibility of venous stasis as a pathogenesis of this kind of hearing loss. The predominance of degenerative changes in the apical region of the cochlea is puzzling. A probable explanation is that radiating veins draining the cochlear coils into the common cochlear vein in the modiolus have a longer course near the apex of the cochlea. Similarly, the radiating arterioles have a longer course in the apical region. Hypoxia arid venous stasis seem more likely to occur in the apex of the cochlea than in its base. Cochlear otosclerosis is known to cause sensorineural hearing loss (Linthicum, 1972). The inner ear structure most commonly involved by otosclerosis is the spiral ligament (Schuknecht, 1974). This ligament shows severe atrophic changes, especially in areas adjacent to otosclerotic foci (Fig. 13). Ruedi and Spoendlin (1966) and Johnsson et al. (1978) suggested the presence of venous shunts between the otosclerotic foci and the venules of the scala tympani. The resulting venous stasis may be the cause of sensorineural hearing loss. Atrophy of the Stria Vascularis in 20 sars of Presbycusis with Flat Audiometric Pattern
30 27 -
I I
24 -
18 -
More than 50% Atrophy
"I!
I I
I:
21 -
Less than 60% Atrophy
:n
in.
33 -
• H
15 12 9 -
6-
•
3-
I
2
3
4
5
6
•
•
7
8
9
10
II
12
13
14
IS
16
17
18
19
20
Number of e a r s
FIG. 12 Graph of the extent of strial atrophy in the cochleas of 20 ears from 15 individuals with flat audiometric patterns of sensorineural hearing loss.
966
A. BELAL
FIG. 13 Otosclerosis in a 27-year-old female. The otosclerotic focus involved the bony labyrinth and the entire footplate of the stapes. Hyalinization and severe degenerative changes appear in the spiral ligament.
Cochlear revascularization
The earliest attempt to increase labyrinthine circulation is attributed to Biancalanca, who in 1939 performed a cervical sympathectomy to treat Meniere's disease. Since then, sympathectomy has been performed to treat a variety of inner ear problems, such as sudden hearing loss, labyrinthine ischaemia, fluctuating hearing loss, gradual sensorineural hearing impairment, allergy of the inner ear and tinnitus. The second phase of revascularizing the cochlea began with attempts to graft the cochlea. House and Glasscock (1969) revascularized the cochlea through a middle fossa approach. Using a diamond burr and suction irrigation, they skeletonized the cochlea between the internal auditory canal and the internal carotid artery. A muscle flap from the tensor tympani was used to revascularize the stria vascularis. Fisch (1970), using the same approach, transposed a pedicle flap of the temporalis muscle over the contents of the internal auditory canal. He named the operation 'meato-myo-syngiosis'. In 1978, he reported the results in 25 cases observed over a three-year period. Six cases had improved hearing, while hearing stabilized in the rest. Ried (1973) and Del Bo (1976) also tried onlay patch grafting of the cochlea. Through a transmeatal approach, the bone over the promontory was thinned and a mucosal flap was brought into contact with the exposed stria vascularis.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR 9 6 7
To date, there is no definite clinical or histopathological evidence that shows the success of these procedures in revascularizing an already 'devascularized ossified cochlea'. The best candidates for cochlear revascularization seem to be patients undergoing surgery that will eventually interfere with the blood supply to the inner ear. House (1971) suggested a first stage cochlear revascularization in patients undergoing acoustic tumour removal. It is hoped that this report will stimulate experimental studies to evaluate the possibility of revascularizing the cochlea, both before and after cutting its blood supply. The similarity between myocardial and cochlear revascularization is striking. The former has passed through three phases: autonomic nervous system surgery, graft onlay surgery and coronary bypass surgery. The latter has already passed the first phase and is now in the second phase. Hopefully in the future we will know whether labyrinthine bypass surgery is possible. Summary
Occlusion of the anterior vestibular artery has resulted in severe degeneration and new bone formation limited to the utricle, saccule, and superior and lateral semicircular canals. Depriving the inner ear of its main blood supply, i.e. the internal auditory artery, has resulted in severe degeneration and ossification of the entire membranous labyrinth, except the endolymphatic duct and sac. A more severe cochlear sclerosis was seen when both arterial and venous blood supplies to the cochlea were occluded. The implications of these findings on the etiology and management of inner ear disorders are emphasized. Acknowledgements
The author would like to thank James Sheehy, M.D., and Fred Linthicum, M.D., for revising the paper, and Diane Foster for editing it. REFERENCES BELAL, A., LINTHICUM, F., and HOUSE, W. (1979a) Submitted for publication. BELAL, A., LINTHICUM, F., and HOUSE, W. (1979b) Submitted for publication.
BIANCALANCA, L. (1939) Minerva Medica, 1, 497. DEL BO, M. (1976) Ada Otorhinolaryngologica Belgica, 30, 407. FffiANDT, H. VON, and SAXEN, A. (1937) Acta Otolaryngologica, Supplement 23. FBCH, U. (1970) Advances in ORL, 17, 203. FISCH, U. (1978) Third International Course of Otoneurosurgery, Grenoble, France. FOWLER, E. (1950) Annals of Otology, Rhinology and Laryngology, 59, 980. GOLDING-WOOD, P. (1969) Journal of Laryngology and Otology, 74, 915 HANSEN, C. (1971) Arch, klin, exp. ohr.- nas.- u. kehlk, Heilk, 200, 83. HILGER, J., and GOLTZ, N. (1951) Laryngoscope, 616, 97.
HOUSE, W. (1971) Laryngoscope, 86, 816. HOUSE, W., and GLASSCOCK, M. (1969) Archives of Otolaryngology, 30,15. JOHNSSON, L. G. (1954) Archives of Otolaryngology, 59, 492. JOHNSSON, L. G. (1973) Advances in ORL, 20, 191.
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JOROENSEN, M. (1961) Archives of Otolaryngology, 74, 164. LINDSAY, J., and HEMENWAY, W. (1956) Annals of Otology, Rhinology and Laryngology, 65,692. LINTHICUM, F. (1972) Archives of Otolaryngology, 95, 564. MAZZONI, A. (1970) Annals of Otology, Rhinology and Laryngology, 81, 13. PAPARELLA, A., and SUGIURA (1967) Annals of Otology, Rhinology and Laryngology, 76, 554 PASSE, E. G. (1953) Archives of Otolaryngology, 57, 257. PERLMAN, H., and KIMURA, R. (1957) Annals of Otology, Rhinology and Laryngology, 66, 537. PERLMAN, H., KIMURA, R., and FERNANDEZ, C. (1959) Laryngoscope, 69, 591.
RED, E. (1973) Ada Otolaryngologica Ibero-Americana, 24, 580. RUEDI, L., and SPOENDLIN, H. (1966) Annals of Otology, Rhinology and Laryngology, 75, 525. SCHUKNECHT, H. (1964) Archives of Otolaryngology, 80, 369. SCHUKNECHT, H., KIMURA, R., and NAUFAL, P. (1973) Acta Otolaryngologica, 76, 75.
SCHUKNECHT, H. F. (1974) Pathology of the Ear. Harvard Press, Cambridge. SCHUKNECHT, H., KIMURA, R., BELAL, A. et al. (1974) Laryngoscope, 84,1777.
SHEEHY, J. (1960) Laryngoscope, 70, 885. SHEEHY, J. (1975) Journal of the Otolaryngological Society of Australia, 4, 3. SILVERSTEIN, H., and MAKIMOTO, K. (1973) Laryngoscope, 83, 1414.
SMITH, C. (1954) Annals of Otology, Rhinology and Laryngology, 63, 435. Reprint requests should be sent to: A. Belal, Jr., M.D., Ear Research Institute, 256 South Lake Street, Los Angeles, California, 90057.
The effects of vascular occlusion on the human inner ear By A. BELAL, Jr., M.D.* (Los Angeles, California) DISORDERS of microcirculation, which are well documented in areas other than the inner ear, might be expected to develop in the inner ear despite the lack of documentation. Von Fieandt and Saxen (1937) described two types of inner ear pathology in old age: senile atrophy of the spiral ganglion and angiosclerotic degeneration of the inner ear. The latter condition is marked by thickening of strial and other cochlear vessels and loss of capillaries followed by sensorineural degeneration. Jorgensen (1961) described a close relationship between cochlear angiopathy and atherosclerosis of the blood vessels in the base of the skull, as well as generalized atherosclerosis. Schuknecht (1964) was the first to draw attention to the effect of strial atrophy on hearing thresholds. Johnsson (1973), who used the surface preparation technique to study human cochlear blood vessels, found that strial atrophy was a common denominator in sensorineural hearing loss. It is tempting for the clinician to assume that many inner ear disorders are caused by vascular pathology affecting the blood supply to the ear. This assumption is the basis of treatment for Meniere's disease, sudden deafness, tinnitus, and other conditions. A vasodilator regimen of intravenous histamine, sublingual and intramuscular histamine, nicotinic acid, probanthine, and benadryl may be prescribed (Sheehy, 1975), or sympathectomy may be performed (Passe, 1953; Johnsson, 1954; GoldingWood, 1969). However, the otologist must remember that histological evidence of vascular pathology in these conditions remains almost completely lacking. This paper is the first review of the effects of depriving the human inner ear of its blood supply. The temporal bones of two patients who had undergone middle fossa surgery—one for vestibular nerve section in Meniere's diseaseand onefor removal of an acoustic tumour—during which the blood supply to the inner ear was deliberately cut, were studied. Both sets of bones have been recently reported (Belal et ah, 1979 a and b respectively). Findings are correlated with the vascular pathology of inner ear problems.
Arterial blood supply of the inner ear
It is generally agreed that only one vessel, the internal auditory artery, supplies the human inner ear. Although there are great variations in the * Research Fellow (1978-1979), Ear Research Institute, Los Angeles, California, and Assistant Professor of Otolaryngology, Alexandria Medical School, Alexandria, Egypt. 955
956
A. BELAL
origin, size, length, course, and ramification of this vessel (Mazzoni, 1970), it divides characteristically into the common cochlear artery and the anterior vestibular artery. The common cochlear artery divides into the main cochlear and vestibulocochlear branches. The latter divides into the posterior vestibular artery and the cochlear ramus (Fig. 1). The usual distribution of these vessels is as follows: The main cochlear artery supplies three-fourths of the cochlea, while the cochlear ramus supplies the basal one-fourth. The anterior vestibular artery supplies the superior surfaces of the utricle, saccule, and superior and lateral semicircular canals. The posterior vestibular artery supplies the posterior semicircular canal and the inferior surfaces of the utricle and saccule. Venous drainage of the inner ear
The venous drainage of the inner ear has been described in detail by Schuknecht (1974). The main veins of the cochlea are the posterior and anterior spiral veins. The posterior vein drains the scala media (external wall), scala vestibuli and spiral ganglia. The anterior vein drains the spiral lamina and scala tympani. These two veins join near the base of the
Wear Duct
FIG. 1 Diagram of the arterial blood supply of the inner ear.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR
957
cochlea to form the common modiolar vein. This is joined in turn by the vestibulocochlear vein to become the vein at the cochlear aqueduct. This main venous channel runs along the cochlear aqueduct to empty into the inferior petrosal sinus. The vestibular labyrinth is drained by the anterior and posterior vestibular veins. These veins join the vein of the round window to become the vestibulocochlear vein. In addition, the semicircular canals are drained by veins that form the vein of the vestibular aqueduct. This accompanies the endolymphatic duct and drains into the lateral sinus. Effect of anterior vestibular artery occlusion
Silverstein and Makimoto (1973), in two sets of experiments on cats, sectioned the superior vestibular and singular nerves and their accompanying vessels in one experiment and only the nerves in the other. Severe degenerative changes in the vestibular labyrinth occurred only in the first instance. Lindsay and Hemenway (1956) described a syndrome of sudden onset of severe vertigo without deafness that gradually resolved in a matter of weeks. This was followed by positional vertigo persisting for weeks or years. The authors suspected the syndrome to be due to occlusion of the anterior vestibular artery. Our study of the previously cited temporal bone (Belal et al., 1979a) found severe degeneration of the utricular and saccular maculae and the cristae of the lateral and superior semicircular canals (Fig. 2). Both canals were filled with fibrous and osteoid tissue. The rest of the membranous labyrinth looked normal (Fig. 3). Figure 4 depicts the effects of blockage of the anterior vestibular artery on the human inner ear. Effect of internal auditory artery occlusion
Perlman et al. (1959) showed that occlusion of the internal auditory artery in guinea-pigs for five minutes produced spotty, degenerative changes in the cochlea, principally in the hair cells and spiral ganglia. Damage to hair cells was severe in the basal turn of the cochlea. Permanent obstruction of the arterial blood supply caused disintegration of the cochlea to begin immediately, with complete necrosis occurring within 24 hours. Progressive fibrosis and ossification of the cochlear spaces followed. The effects of internal auditory artery occlusion on the human ear were illustrated in the previously cited temporal bone (Belal et al., 1979b). Because the internal auditory artery was sacrificed during surgery, the patient completely lost his hearing. Histopathological examination showed severe degenerative changes and ossification of the cochlea and the entire vestibular labyrinth (Fig. 5). Cochlear ossification was pronounced in the basal and middle turns. In addition, ossification involved only the scala tympani (Fig. 6). All turns of the scala vestibuli were free of new bone
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A. BELAL
Fto. 2 The superior vestibular nerve and the anterior section. nerve r vestibula Right middle fossa t e the m a r k Servin to d n a l ery superior v e s S * ™ " t hise denervat ^ '*£The "*'• ^ f nerve. ormath nefve"r ed and new bone formation appears in the utricle the ffac.al nerve from lateral semicircular canal.
u^gTiv.-Inferio r V&rjtii>u\ii • - < ' Nerve FIG. 3 r and singular nerves were cut. The saccule is vestibula inferior Same case as in Fig. 2. The ng of Reissner's denervated and collapsed. The cochlea looks normal except for the ballooni membrane in the apical coil.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR
959
ochlear Duct
FIG. 4 Diagram of the effects of anterior vestibular artery occlusion on the human inner ear.
formation. Ossification and degeneration pervaded the vestibular labyrinth except for the endolymphatic duct and sac, which appeared normal (Fig. 7). The pattern of cochlear ossification after arterial blood supply deprivation seems to be related to the anatomy of venous drainage of the cochlea. Smith (1954) has shown that the radiating arterioles supplying the cochlea arise at regular intervals from the common cochlear artery. These arterioles pass over the scala vestibuli and scala media to form capillaries, which are drained by collecting venules in the lower part of the spiral ligament. Thus, the main venous drainage crosses over the scala tympani. The cochlear venous channels run caudalward from apex to base to drain into the vein of the cochlear aqueduct. Ossification presumably occurs due to haemorrhage in the perilymphatic spaces. Haemorrhage starts in cochlear areas with good access to venous nonoxygenated blood. This substantiates the theory that labyrinthine ossification occurs from perivascular or adventitial cells around capillaries (Paparella and Sugiura, 1967). These undifferentiated mesenchymal cells give origin to osteoblasts that induce new bone formation. The possibility of arteriolar anastomosis between the middle ear
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A. BELAL
Remnant of Acoustic Neuroma
Ossified Vestibule Ossified Lateral 'Degenerated Cochtear Nerve
FIG. 5 Right middle fossa removal of acoustic tumour. The internal auditory artery was cut during the operation. Degeneration and ossification cover the entire inner ear except for the apical coils of the cochlea and ths endolymphatic duct and sac. The cochlear nerve has degenerated, and a remnant of the tumour remains in the antero-inferior compartment of the internal auditory canal.
Degenerated Organ Of Cortr
FIG. 6 Same case as in Fig. 5. The basal coil of the cochlea shows new bone formation in the scala tympani, modiolus and spiral ligament. The sensorineural structures have completely degenerated.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR
Posteri o r Fossa FIG. 7 Same case as in Fig. 5. Endolymphatic duct and sac are normal.
Endotymphatic-p
^ ^Anastomoses ?
hlear Duct
FIG. 8 Diagram of the effects of internal auditory artery occlusion on the human inner ear.
961
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A. BELAL
in promontory, otic capsule and apical half of the cochlea should be kept area,' key lar 'Vascu the as mind. Hansen (1971) described this anastomosis the a highly vascularized area of endochondral bone situated between canal y auditor l interna and cochlea, vestibule, middle ear, promontory sac fundus. The normal appearance of the endolymphatic duct and the of dura the from supply blood suggests the presence of a collateral rative degene of ution distrib the shows 8 posterior cranial fossa. Figure changes in the inner ear after internal auditory artery occlusion. Effect of arterial and venous occlusion on the cochlea
Perlman and Kimura (1957), obstructing the venous drainage in animal studies, found that degeneration of the outer hair cells was evident within 24 hours and the number of ganglion cells was reduced within two weeks. first The stria vascularis was particularly susceptible, often showing the days seven to up seen signs of damage. Haemorrhages were commonly ve after obstruction. Subsequent fibrosis and ossification were less extensi tion. obstruc with venous obstruction than with arterial Effects of occlusion of the arterial blood supply and of venous drainage of the cochlea were seen in the temporal bones of five patients who underwent a translabyrinthine removal of cerebellopontine angle tumours. With the this surgery, both the arterial blood supply and the venous drainage of
Facial Nerve
i 9 . The arterial supply and venous drainage neuroma acoustic of Left translabyrinthine removal sclerosis is total. of the cochlea were presumably cut in the course of surgery. Cochlear FIG.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR
963
cochlea are cut. The temporal bones showed total osseus sclerosis of the cochlea (Fig. 9). Ossification involved all the scalae of the cochlear duct and all the cochlear turns were similarly ossified (Fig. 10). Thus, it seems that occlusion of both arterial and venous blood channels results in more severe degeneration and sclerosis of the cochlea than arterial occlusion alone. Ischemic changes presumably occur early, so that anastomotic channels do not have sufficient time to develop. Probable vascular etiology of inner ear diseases
Histopathological changes that have been described should be evaluated critically. Vascular effects could be secondary to the primary pathology in the inner ear or to the surgical procedure undertaken to treat it. However, histopathological studies did not focus on the microvascular network of the inner ear because it is not clearly seen in conventional celloidin sections. Given this limitation, the observations presented suggest important implications for vascular diseases of the inner ear and their treatment. The most common of these diseases is sudden sensorineural hearing impairment. The two most popular concepts to explain this condition are viral labyrinthitis (Schuknecht et al., 1973) and vascular occlusion (Fowler, 1950; Hilger and Goltz, 1951; Sheehy, 1960). To date, all pathological
FIG. 10 Same case as in Fig. 9. Bone totally obliterates the apical and middle turns of the cochlea.
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material from temporal bones of patients with this disease shows a situation different from what we have described. The most consistent pathological change in these bones is atrophy of the organ of Corti. No temporal bones have shown fibrous or bony proliferation in the inner ear. Although vascular conditions, such as leukaemia, Buerger's disease and macroglobulinaemia, can produce sudden hearing loss, most cases are due to viral, rather than vascular, etiology. Thus, a vasodilator regimen seems unlikely to have value in the treatment of most of these cases. The similarity of the pattern of cochlear sclerosis associated with labyrinthitis ossificans and that associated with deprivation of blood supply (Fig. 11) seems to be more than coincidental. Labyrinthitis ossificans is the healed stage following labyrinthitis, whether otic or meningitic in origin. New bone formation in these cases seems to be due to deprivation of the blood supply to the membranous labyrinth. Septic embolization, followed by haemorrhages in the perilymphatic spaces, is a probable explanation for the pathogenesis of new bone in the labyrinth. Atrophy of the stria vascularis is a common cause of hearing loss that is bilateral and symmetrical, with flat audiometric patterns and excellent speech discrimination (Schuknecht et al., 1974). The temporal bones of persons with this type of hearing loss show atrophic changes in the stria vascularis, most of which are localized in the apical regions of the cochlea
FIG. 11 Labyrinthitis ossificans. There is total osseous sclerosis of the cochlea. The labyrinthine spaces and modiolus have been replaced by lamellar bone. The borders of the new bone can be readily distinguished from the surrounding otic capsule.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR 965
(Fig. 12). The resemblance between these findings and those following venous obstruction (Kimura and Perlman, 1956) suggests the possibility of venous stasis as a pathogenesis of this kind of hearing loss. The predominance of degenerative changes in the apical region of the cochlea is puzzling. A probable explanation is that radiating veins draining the cochlear coils into the common cochlear vein in the modiolus have a longer course near the apex of the cochlea. Similarly, the radiating arterioles have a longer course in the apical region. Hypoxia arid venous stasis seem more likely to occur in the apex of the cochlea than in its base. Cochlear otosclerosis is known to cause sensorineural hearing loss (Linthicum, 1972). The inner ear structure most commonly involved by otosclerosis is the spiral ligament (Schuknecht, 1974). This ligament shows severe atrophic changes, especially in areas adjacent to otosclerotic foci (Fig. 13). Ruedi and Spoendlin (1966) and Johnsson et al. (1978) suggested the presence of venous shunts between the otosclerotic foci and the venules of the scala tympani. The resulting venous stasis may be the cause of sensorineural hearing loss. Atrophy of the Stria Vascularis in 20 sars of Presbycusis with Flat Audiometric Pattern
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FIG. 12 Graph of the extent of strial atrophy in the cochleas of 20 ears from 15 individuals with flat audiometric patterns of sensorineural hearing loss.
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FIG. 13 Otosclerosis in a 27-year-old female. The otosclerotic focus involved the bony labyrinth and the entire footplate of the stapes. Hyalinization and severe degenerative changes appear in the spiral ligament.
Cochlear revascularization
The earliest attempt to increase labyrinthine circulation is attributed to Biancalanca, who in 1939 performed a cervical sympathectomy to treat Meniere's disease. Since then, sympathectomy has been performed to treat a variety of inner ear problems, such as sudden hearing loss, labyrinthine ischaemia, fluctuating hearing loss, gradual sensorineural hearing impairment, allergy of the inner ear and tinnitus. The second phase of revascularizing the cochlea began with attempts to graft the cochlea. House and Glasscock (1969) revascularized the cochlea through a middle fossa approach. Using a diamond burr and suction irrigation, they skeletonized the cochlea between the internal auditory canal and the internal carotid artery. A muscle flap from the tensor tympani was used to revascularize the stria vascularis. Fisch (1970), using the same approach, transposed a pedicle flap of the temporalis muscle over the contents of the internal auditory canal. He named the operation 'meato-myo-syngiosis'. In 1978, he reported the results in 25 cases observed over a three-year period. Six cases had improved hearing, while hearing stabilized in the rest. Ried (1973) and Del Bo (1976) also tried onlay patch grafting of the cochlea. Through a transmeatal approach, the bone over the promontory was thinned and a mucosal flap was brought into contact with the exposed stria vascularis.
THE EFFECTS OF VASCULAR OCCLUSION ON THE HUMAN INNER EAR 9 6 7
To date, there is no definite clinical or histopathological evidence that shows the success of these procedures in revascularizing an already 'devascularized ossified cochlea'. The best candidates for cochlear revascularization seem to be patients undergoing surgery that will eventually interfere with the blood supply to the inner ear. House (1971) suggested a first stage cochlear revascularization in patients undergoing acoustic tumour removal. It is hoped that this report will stimulate experimental studies to evaluate the possibility of revascularizing the cochlea, both before and after cutting its blood supply. The similarity between myocardial and cochlear revascularization is striking. The former has passed through three phases: autonomic nervous system surgery, graft onlay surgery and coronary bypass surgery. The latter has already passed the first phase and is now in the second phase. Hopefully in the future we will know whether labyrinthine bypass surgery is possible. Summary
Occlusion of the anterior vestibular artery has resulted in severe degeneration and new bone formation limited to the utricle, saccule, and superior and lateral semicircular canals. Depriving the inner ear of its main blood supply, i.e. the internal auditory artery, has resulted in severe degeneration and ossification of the entire membranous labyrinth, except the endolymphatic duct and sac. A more severe cochlear sclerosis was seen when both arterial and venous blood supplies to the cochlea were occluded. The implications of these findings on the etiology and management of inner ear disorders are emphasized. Acknowledgements
The author would like to thank James Sheehy, M.D., and Fred Linthicum, M.D., for revising the paper, and Diane Foster for editing it. REFERENCES BELAL, A., LINTHICUM, F., and HOUSE, W. (1979a) Submitted for publication. BELAL, A., LINTHICUM, F., and HOUSE, W. (1979b) Submitted for publication.
BIANCALANCA, L. (1939) Minerva Medica, 1, 497. DEL BO, M. (1976) Ada Otorhinolaryngologica Belgica, 30, 407. FffiANDT, H. VON, and SAXEN, A. (1937) Acta Otolaryngologica, Supplement 23. FBCH, U. (1970) Advances in ORL, 17, 203. FISCH, U. (1978) Third International Course of Otoneurosurgery, Grenoble, France. FOWLER, E. (1950) Annals of Otology, Rhinology and Laryngology, 59, 980. GOLDING-WOOD, P. (1969) Journal of Laryngology and Otology, 74, 915 HANSEN, C. (1971) Arch, klin, exp. ohr.- nas.- u. kehlk, Heilk, 200, 83. HILGER, J., and GOLTZ, N. (1951) Laryngoscope, 616, 97.
HOUSE, W. (1971) Laryngoscope, 86, 816. HOUSE, W., and GLASSCOCK, M. (1969) Archives of Otolaryngology, 30,15. JOHNSSON, L. G. (1954) Archives of Otolaryngology, 59, 492. JOHNSSON, L. G. (1973) Advances in ORL, 20, 191.
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JOROENSEN, M. (1961) Archives of Otolaryngology, 74, 164. LINDSAY, J., and HEMENWAY, W. (1956) Annals of Otology, Rhinology and Laryngology, 65,692. LINTHICUM, F. (1972) Archives of Otolaryngology, 95, 564. MAZZONI, A. (1970) Annals of Otology, Rhinology and Laryngology, 81, 13. PAPARELLA, A., and SUGIURA (1967) Annals of Otology, Rhinology and Laryngology, 76, 554 PASSE, E. G. (1953) Archives of Otolaryngology, 57, 257. PERLMAN, H., and KIMURA, R. (1957) Annals of Otology, Rhinology and Laryngology, 66, 537. PERLMAN, H., KIMURA, R., and FERNANDEZ, C. (1959) Laryngoscope, 69, 591.
RED, E. (1973) Ada Otolaryngologica Ibero-Americana, 24, 580. RUEDI, L., and SPOENDLIN, H. (1966) Annals of Otology, Rhinology and Laryngology, 75, 525. SCHUKNECHT, H. (1964) Archives of Otolaryngology, 80, 369. SCHUKNECHT, H., KIMURA, R., and NAUFAL, P. (1973) Acta Otolaryngologica, 76, 75.
SCHUKNECHT, H. F. (1974) Pathology of the Ear. Harvard Press, Cambridge. SCHUKNECHT, H., KIMURA, R., BELAL, A. et al. (1974) Laryngoscope, 84,1777.
SHEEHY, J. (1960) Laryngoscope, 70, 885. SHEEHY, J. (1975) Journal of the Otolaryngological Society of Australia, 4, 3. SILVERSTEIN, H., and MAKIMOTO, K. (1973) Laryngoscope, 83, 1414.
SMITH, C. (1954) Annals of Otology, Rhinology and Laryngology, 63, 435. Reprint requests should be sent to: A. Belal, Jr., M.D., Ear Research Institute, 256 South Lake Street, Los Angeles, California, 90057.
