- Email: [email protected]
Pathologic significance of Meniere's symptom complex
Pathologic Significance of Meniere's Symptom Complex A Histopathologic and Electron Microscopic Study AZIZ BELAL, IR., M.D.,* AND JUKEA YLIKOSKI, M.D.+
Histologic and ultrastructural findings in the temporal bones cf a patient clinically diagnosed as having unilateral Meniere's disease are presented. The patient underwent two endolymphatic subarachnoid shunt operations that failed to relieve symptoms and a middle fossa vestibular nerve section that completely relieved episodic vertigo and stabilized hearing in the ear operated upon. Histopathologic examination of the temporal bones shewed no endolymphatic hydrops in either ear, The maculae and cristae on the side operated upon showed severe degenerative changes attributed to vestibular neurectomy. The cochleograms of the operated and contralateral ears showed degeneration of the sensorineural structures in the basa~ two turns of the cochlea. No apparent cause for the fluctuant hearing loss was found in the cochlea or the cochlear nerve of the involved ear, Light and electron microscopic studies of the vestibular nerve excised at the time of vestibular neurectomy showed that most of the nerve fibers and ganglion cells were essentially normal. Collagen tissue deposition was increased in some areas of the endoneurial space. Most myelinated nerve fibers in these areas had degenerated. Although these changes may be partly due to artifacts and partly due to aging, they probably are the result of a pathologic process affecting the vestibular nerve, These findings suggest that a revised approach to the etiology, pathogenesis, and treatment of Meniere's symptom complex is indicated_
Meniere's disease is characterized by vertiginous episodes, hearing loss, and tinnitus. Alfaro' added fullness and pressure sensation to this symptom complex. The vertiginous episodes usually have a sudden onset, reach maximal intensity within a few minutes, last for an hour or more, and either subside completely or continue as a sensation of imbalance for hours or days. The hearing loss is sensorineural and is characterized by loudness recruitment and decreased speech discrimination scores. There are
fluctuations in hearing, usually for the low frequencies. Tinnitusmay be paroxysmal or constant, varied in pitch and intensity, and increased in severity just before the onset of the vertiginous attack. In the typical attack, pressure sensation and cochlear symptoms precede vertigo. This characteristic presentation of Meniere's disease is not always seen in clinical practice, primarily because of two factors. First, there are atypical forms of Meniere's disease. The each-
Accepted for publication March 26, 1980. *Assistant Professor of Otolaryngology, Alexandria Medicnl School, Alexandria, Egypt. Research Fellow, Ear Itesearch Institute, Los Angeles, California. tAssociatc Professor of Otoloryngology. University of Helsinki,.Helsinki, Finland. Visiting Professor, Ear Research Institute. Los Angeles, California. American Journal of Otolaryngology --Volume 1, Number 4, August 1980
275
American Journal of Otolaryngology
lear form is characterized by fluctuating hearing loss, tinnitus, a n d pressure, b u t no vertigo. Vestibular Meniere's disease p r o d u c e s vertigo, tinnitus, and pressure, but no hearing loss. In Lermoyez's syndrome, fluctuations in hearing occur in reverse relationship to the vertiginous episode; i.e., hearing is i m p r o v e d during and immediately after the attack. In Tumarkin's attacks, the patient experiences an abrupt falling sensation of fleeting duration. Second, two clinical forms, the compensated and u n c o m p e n s a t e d , ensue during the natural course of Meniere's disease. ~ In the compensated form, the vertiginous attack is preceded by increased pressure sensation, tinnitus, and hearing loss. As the frequency of the attacks increases, they u s u a l l y become shorter and occur with fewer warning signs. The pure tone levels tend to drop, a n d speech discrimination does not completely return b e t w e e n attacks. During the decompensated form of the disease, the hearing in the involved ear drops and tinnitus and ear discomfort are continuous. Vertiginous attacks usually occur without warning. The presence of t w o or more diseases complicates the clinical picture even more. Presbycusis and noise i n d u c e d hearing loss are frequently associated with Meniere's disease or other causes of vertigo. This article reports the histopathologic findings in a patient with typical signs and symptoms of Meniere's disease as defined by the Subcommittee on Hearing a n d Equilibrium of the American A c a d e m y of Ophthalmology and Otolaryngology. 3 The clinical diagnosis was unilateral Meniere's disease. The patient underwent two endolympllatic subarachnoid shunt procedures that were unsuccessful in alleviating symptoms and a successful middle fosse vestibular nerve section. Histologic examination of the temporal bones and electron microscopic examination of the vestibular nerves excised at surgery failed to s h o w the cause of the symptoms. The histopathologic findings relating to the endolymphatic subarachnoid shunt operations and vestibular n e u r e c t o m y have been previously reported.4, s
METHODS
AND
MATERIALS
A 62 year old w o m a n was first examined at the Otologic Medical Group, Inc., in May 1971. She had had attacks of dizziness for at least six years. The first attack w a s violent, associated with 276
nausea and vomiting, and persisted for a few days. Attacks occurred every few months. She had fluctuant hearing loss that was more prominent in the right ear than in the left. She also complained of fullness and constant tinnitus of fluctuating intensity in the right ear. Physical examination revealed intact mobile tympanic membranes. The Weber test revealed lateralization to the left ear. There was a 45 dB. average hearing loss with 88 per cent speech discrimination scores in the right ear and a 40 dB. average hearing loss and 92 per cent discrimination scores in the left. B6k6sy tracings and the short increment sensitivity index were compatible with a cochlear lesion in the right ear. Radiographic examination showed normal internal auditory canals bilaterally. Caloric testing with electronystagmography demonstrated directional preponderance to the left. The fluorescent treponemal antibody absorption test was negative. The five hour glucose tolerance test showed a flat curve. A thyroid profile was normal. A diagnosis of right Meniere's disease was made. A vasodilator regimen composed of intravenous doses of histamine, niacin, and'sublingual and subcutaneous doses of histamine was prescribed, b u t the patient continued to be dizzy. A right endolymphatic subarachnoid shunt operation was performed in July 1971. With the patient under general anesthesia, a long silicone rubber shunt tube was inserted between a large, well developed endolymphatic sac and the subarachnoid space. After surgery, dizziness lessened, tinnitus worsened, and hearing levels remained about the same. One year postoperatively spinning attacks recurred. In October 1972 a revision right endolymphatic subarachnoid shunt operation was done with the patient under local anesthesia. The shunt tube, found closed in the endolymphatic sac area, was replaced by another tube that allowed good flow of cerebrospinal fluid. The patient remained free of symptoms for one year, after which she reverted to a pattern of frequent dizzy spells, nausea, and vomiting. Hearing levels in the right ear fluctuated from 48 to 55 dB. average loss. Speech discrimination scores fluctuated b e t w e e n 76 and 92 per cent. In December 1973 a right middle fassa vestibular nerve section was done. With the patient under general anesthesia, the internal auditory canal was exposed by removing bone over the geniculate ganglion and superior semicircular canal. The facial nerve canal was followed and the internal auditory canal opened. The macroscopic appearance of the compartments of the inter-
PATHOLOGIC SIGNIFICANCE OF MENIERE'S SYMPTOMCOMPLEX
hal auditory canal was normal. The superior and inferior vestibular nerves were identified and sectioned separate]y proximal to Scarpa's ganglion, and the distal segments of the nerves were removed. These specimens were immediately fixed in cold 3 per cent Karnovsky's solution overnight, postfixed in 1 per cent osmium tetroxide, processed by alcohol dehydration, and embedded in Epon. One micron thick sections were stained with toluidine blue 0 for light microscopy and thin sections with uranyl acetate and lead citrate for electron microscopy. Postoperatively the patient had mild facial weakness that completely resolved during the next two months. Dryness of the right eye required a tarsorrhaphy. The dizzy spells were completely relieved, although she had some unsteadiness when arising or walking. Tinnitus improved. Audiometric testing, repeated two and eight months postoperatively, showed a 10 dB. improvement in the low tones. Retesting 20 months postoperatively showed regression of auditory function to the preoperative level.
h~ June 1976 the patient died at age 67 of unrelated causes. The autopsy report was not available, and the death-autospy period is unknown. Both temporal bones were acquired at autopsy, fixed in formaldehyde, dehydrated, embedded in celloidin, and sectioned at 20 microns' thickness. Each tenth section was stained with hematoxylin and eosin.
Volume 1 Number 4 August 1780
HISTOPATHOLOGIC FINDINGS The right temporal bone s h o w e d an intact middle ear, tympanic membrane, and ossicles. Bone debris embedded in fibrous tissue was seen in the region of the stapes. The mastoid bone was well pneumatized and showed an operative cavity lined with fibrous tissue. Although the endothelial lining of the endolymphatic sac was identified, the continuity b e t w e e n the area occupied by the flange of the shunt tube and the lining of the sac could not be followed. However, there was minimal fibrosis in the shunt area.
Figure 1. Right temporal bone in which the middle fossa vestibular nerve section had b e e n performed. The superior vestibular nerve was sectioned. The vartleal bony bar (Bill's bar) is the landmark serving to separate the superior vestibular nerve from the facial nerve. The utricle is denervated, and bone formation has occurred i n the lateral semicircular canal.
AZIZ BELAL, JR., AND JUKKA YLIKOSKI
27 7
American
Journa] of Otolaryngology
Figure 2. Rtght temporal bone in w h i c h the middle fossa vestibular nerve section had been performed, The inferior vestibular nerve was sectioned. The saccule is denervated and collapsed. There is herniation of Reissner's membrane in the h o o k region of the cochlear duct into the vestibule where it lies in contact with t h e footplate of the stapes. Bone dust in the region of the stapes was presumably the result of e n d o l y m p h a t i c shunt operations.
Figure 3.
278
Apical coil of the r i g h t cochlea showing a slight outward displacement of Reissner's membrane,
PATHOLOGIC SIGNIFICANCE OF MENIERE'S SYMPTOM COMPLEX
The internal auditory canal showed a surgical defect, which was closed partially by periosteal new hone formation and partially by fibrous tissue. The superior and inferior vestib!flar nerves, presumably excised at the time of vestibular neurectomy, were almost totally replaced by fibrous tissue (Figs. 1, 2). The facial and cochlear nerves appeared to be intact. Few Scarpa's ganglion cells could be identified in the internal auditory canal. The geniculate ganglion and the greater superficial petrosal nerve appeared to be normal. The superior and lateral semicircular canals were filled with fibrous and osteoid tissue that almost completely obliterated their lnmina. The ampullae and neuroepithe[ia of the cristae in both canals were denervated. The maculae of the utricle and saccule were also denervated, but the hair cells appeared to be intact. The saccular walls were collapsed over the macula. Although the posterior ampullary nerve was totally degenerated, the crista of the posterior semicircular
canal appeared normal and showed a basophilic deposit over the cupula. The facial nerve appeared to be normal throughout its course. The cochlear duct shewed no endolymphatic hydrops (Fig. 3). Reissner's membrane showed mild displacement outward in the apical coil. There was herniation of Reissner's membrane in the hook region of the cochlea into the vestibule, where it contacted the undersurface of the footplate of the stapes. Cochlear reconstruction showed severe degeneration in the sensorineural structures in the basal 30 millimeters o f the cochlear duct (Fig. 4). The stria vascularis was normal throughout the cochlear duct. The left temporal bone showed an essentially normal middle ear and mastoid. The internal auditory canal showed intact vestibular, facial, and cochlear nerves. The semicircular canal cristae, as well as the maculae of the utric]e and saccule, had normal innervation. The cochlear duct shewed no endolymphatic hydrops, but
o |174
e
~
99
_'=SX'.'. ~
::+_l~'.( .;wp .,.~leeeefe ,
o
ENDORGANS
O~OqI 9
9 .o/|
L
~
o o otdW-
~
,
o\.~
~
.\.,~
.
Ho,
- }~ _'L82 ?I'"
"X::. :):::
m ~
.
sac
~,~..~,._.~...;l else, w / e e l
/
,
~.
August 1980
VESTI BU t A R
'='",~" Q
9O |
Volume 1 Number 4
./..o
.
.
.
s.p
,o,,
0.
. uJ~eo o/_eoo
ooo\. ,':*ks "+"--~" ",.~o=i- j.,NEURONS ~oo\o ', " | 1 7 6 1 7 6 1 7 6 . . . . . . . . . . ~,'-~o ooo\e
",
u u u _-~ _ o o o~'~
~
Figure 4. Right audiogram and cochleograms showing severe degeneration of the sensorineural structures, more manifest in the basal 10 r a m , of the cochlear duct. The stria vascularis appeared normal throughout. All the vestibular end organs, with the exception of the posterior canal ampulla, showed severe degenerative changes.
o
---'"
_
o ~ ooo
5 o~o(
~
Riqht Ear
o
79,~/ooo
HAIR CELLS
~176
| Intact O Absent
%
Frequency In Cycles Per Second
Atrooh~, __
O R G A N OF CORTI
10
SPIRAL GANGLION ,, , , ,
"'
'
~oS~ r--- O-,- 0-~ --!~!/01 ~a
11O;o
7s !
2S i!i!!i!ii!iiiii
75 sea
1ooo 2ooo 4ooo
~ooo
.....
!i!!iiiiiili;iii!i!',!iii,ililill iiiii,
B0
100 +o
.._....1.:<,.
25
I ~3
STRIA VASCULARIS
Normal .L 10
I 20
30
rnm Cochlear D u c t
AZIZ BELAL, JR., AND JUKKA YLIKOSKI
279
Under electron microscopy the majority of the ~,yeli~:atg~,t r_erve ~bers else a;;peared tc ~e normal. Fibers showing total or partial denudation Df the myelin sheath or bizarre disarrangement of myelin were often located among normal nerve fibers (Fig. 7). Irt some areas there was an apparent increase in the endoneurial connective tissue, in w h i c h case myelin sheaths of remaining nerve fibers were severely fragmented and deformed (Fig. 8). The thickness of the myelin sheaths varied considerably; several had only tO to 15 lamellae. All the vestibular ganglion cells were unmyelinated. They appeared Lo be normal except for several lipofuscin inclusions in the cytoplasm (Fig. 9).
there was slight outward displacement of Reissr_er's membrar, e in tke apica ~-co;,[. Cock!ca: reconstruction showed degeneration of the hair cells from the base to the apex and spiral ganglion atrophy in the basal two turns of the cochlea (Fig. 5). The stria vascularis was normal throughout the cochlear duct. Under light microscopy the majority of the myelinated nerve fibers of the vestibular nerve appeared to be normal. The diameters of individual fibers ranged from 1 to 10 microns. Some groups of fibers s h o w e d relatively small diameters. The myelin sheath was deformed in about 20 per cent of the fibers, particularly those lying in the peripheral areas of the nerve. These fibers appeared as swollen, disorganized, dark material completely I~lling the axis cylinder. The appearance of the vestibular ganglion cells was normal. The amount of endoneurial collagen tissue appeared to be increased .both in the ganglion and in the peripheral zones of the nerve (Fig. 6).
American
Journa! of OtolaryngoJegy
9 e 0/~@
O|
9 ~ooe o\ooe
o oo.,,~
OOOlO Ooole |174o le c o o l e 9 o O l e o o Q I= e o o~.^~lT,,
,,~
o~.ooe
..~.~|
,,\ooo
J ~ - " ~ o N
/'/
l:1
_
f.:!
o o o~,bt e o \ o
| o
e~o0|
m ~ , ~ ~ee
= ,, o p o |
NEURONS
This report raises more questions than it provides answers. The absence of histologic proof of endolymphatic hydrops in a case clinically d[ag-
O~OOe
99 o/a 9 9 o/o
@ Q 0/O
DISCUSSION
~2
0 O 0 "%0 -j ~ ~ V
e%ooe eloeo otoee
"~,~"~_
~-~,.
"**~Z ~.~.ZIu
~
e\ooe
25.~ ~ , ~
~
,,~ujooe
"J~'~'Wl~. O
'~e-boe
~ u ~ / ~
-- I-'~'
Figure 5. Left audiogram a n d cochleogrems showing severe degeneration of the sensorineural structures throughout the cochlear duct. The stria vascularis appeared normal throughout the cochlea.
OAbsent
Left
Ear
Frequency In Cycles Per Second
% Atrophy
ORGAN OF CORTI
75 25 ,o
-
_,
so 1
r'-
vs
SPIRAL GANGLION
iii!!{iiiiliiiiiii;ii!iiii ;ii........
60
70
Discriminalion 9 2 ~
so
250
1
500
1000
I
2000 4 0 0 0
STRIA VASCUL ARIS
8000
751 25 0
280
Normal 10
20
mm Cochlear Duct
30
PATHOLOGIC SIGNIFICANCE a t ;' MENIERE'S SYMPTOM COMPLEX
Volume 1 Number 4
August 19B0
Transversesection of vestibular nerve at the level of Scarpa's ganglion shows several ganglion cells and myelinated nerve fibers. The nerve fibersand ganglion cells appear normal, but the amount of endoneurial connective tissue appears increased. [Epoxyembeddedsection. Toluidine blue 0 stain, x350.)
Figure {3.
nosed as Meniere's disease makes the diagnosis questionable. Episodic vertigo with fiuctuant hearing loss, tinnitus, and pressure sensation made this diagnosis inevitable. With no reliable clinical test for endolymphatic hydrops, misdiagnosis and overdiagnosis of Meniere's disease will continue. Klockhoff and Lindblom 6 reported on the glycerol test as a means of diagnosing endolymphatic hydrops. A positive result indicates Meniere's disease; a negative result does not exclude this diagnosis. However, it has recently been shown that psychologic factors play a significant role in the outcome of this testJ Endolymphatic hydrops is not specific for Meniere's disease. In a recent study, endoiymphatic h y d r o p s was found in 9 per cent of 703 temporal bones available in the temporal bone collection of the Ear Research Institute, Los Angeles. s Included were normal ears of two newborns, poststapedectomy ears, and ears from AZIZ BELAL.JR., AND IUKKAYLIKOSKI
patients with the primary diagnosis of Meniere's disease, Paget's disease, hereditary sensorineural hearing loss, congenital syphilis, and chronic otitis media. Only one-third of these patients had exhibited the typical Meniere s y m p t o m complex, i.e., fluctuant hearing loss, episodic vertigo, tinnitus, and pressure in the ear. How, then, can we explain the Meniere symptom complex in the case presented here? If this case was indeed Meniere's disease, can pressure variations in the e n d o l y m p h occur without displacement of Reissner's membrane and of the saccular membranous walls? The membranous walls of the pars superior, i.e., utric]e and semicircular canals, are k n o w n to be less prone to distention in endolymphatic bydrops than the rest of the membranous labyrinth, although the wails have the same histolog~c structure2 Can the degree of elasticity of these membranes vary from one individual to the next, and, accordingly, can histologic manifestations 281
~meFicGrl
Journol of Otolarynsolosy
Figure 7. Low magnification electron micrograph of vestibular nerve.The majority of myelinatedfibers appear normal Som~ nervefibers are swoIlertandhave deformed,disorganized myelin [arrows). [x3600.)
of endalymphatic hydrops vary? In the case presented, outward displacement of Reissner's membrane in the apical coil of the cochlea in both ears as well as herniation of this membrane in the hook region of the operated ear axe histologic t]ndings that were previously recorded in normal temporal bones.U~ If this case was truly Meniere's disease, it is also possible thai the temporal bones reflected spontaneous remission of the disease, or that the shunt procedures and vestibular neurectomy had relieved the increased endolymphatic pressure. However, it has been previously shown both in animal experiments and in h u m a n temporal bone studies that the membranous wails of the labyrinth behave like varicose veins: once dilated, always dilated. TM "-' Now let us suppose that the case is not Meniere's disease. Disease involving the labyrinth cannot be excluded in this case because of the severe degenerative changes, presumably following vestibular neurectomy. These changes were localized mainly to the superior and lateral
282
An area of increased fibrosis in which the endoneurial space shows depositions of eollagenous material. Myetinated nerve fibers in this area show disintegration of their myelin sheaths. (• 3600.]
Figure 8.
semicircular canals. Although the posterior semicircular canal was similarly denervated, its crista appeared to be normal. The distribution of these degenerative changes in the vestibular system foll~ws the distribution of the anterior vestibular artery, which is presumably cut during vestibular neurectomy. LaPerlman et al. j4 showed t h a t occlusion of the internal auditory artery in guinea pigs produced progressive fibrosis and ossification of the labyrinthine spaces. Similar changes were described in h u m a n temporal bones, presumably following occlusion of the labyrinthine blood vessels. L'~,u~ On the other hand, the myelinated nerve fibers of the vestibular nerve in the biopsy specimen showed changes similar to those reported earlier in h u m a n eighth nerve operative specimens from patients with various ear disorders. ~7 T h e deformation of the myelin sheaths, "hyperplastic myelin," is probably caused by compression during specimen handling, and thus probably is an artifact, is Fragmentation of myelin sheaths often seen in areas with increased fibrosis might
PATHOLOGIC SIGNIFICANCEOF MENIERE'S SYMPTOMCOMPLEX
be a pathologic change. Similarly, the relatively abundant, small caliber, thinly myelinated nerve fibers indicate a stage of regeneration of the nerve. ~ Furthermore, in many neuropathies the loss of nerve fibers and subsequently increased endoneurial fibrosis may be only mild. A typical example of such a change is mild chronic compressive neuropathy. Experimental studies of the peripheral nerves have shown that chronic compression causes congestion of the nerve, which further leads to stasis of endoneurial capillaries, damage to capillary endothelial cells due to hypoxia, and leaking of proteins into the endoneurial space, causing swelling. These conditions in turn lead to stimulation of fibroblastic activity and ultimately to increased fibrosis. TM Simultaneously some of the nerve fibers become affected by increased endoneurial pressure, which is histologically characterized by thinning of nerve fibers, segmental demyelination, wallerian degeneration, and other evidence of
regeneration2'."" These changes are accompanied by physiologic alterations. W h e n nerve fibers become hypoxic, at a certain point they become hyperexcitable and begin to discharge spontaneously. '-'a Increased endoneurial fibrosis combined with regenerative changes in vestibular nerves from patients with vertigo of u n k n o w n etiology has recently been observed2 ~ Because m a n y of these patients also had a narrow internal auditory canal or a .space occupying anatomic structure in the canal, the possibility of chronic compression as the etiologic factor in these cases was suggested. In the case presented, the internal auditory canal was radiologically normal, and the compression theory is thus not directly applicable. However, the compression may have been exerted by blood vessels or arachnoid membranes within the internal auditory canal, or the bony narrowing may have occurred only in the most distal part of the canal, in the cribrose area.
Volume 1 Number 4 August 1980
Figure 9. Two culls of Scarpa's ganglion with numerous lipofuscin inclusions in the peripheral cytoplasm [arrows). The cell on the left shews slightly more filamentous elements in the cytoplasm than the cell an the right. Both cells are surrounded by a thin rim of satellite cell cytoplasm (SI with no myelin sheath. N, nucleus (•
AZIZ BELAL,
IR., AND IUKKA YLIKOSKI
283
Arnericun
.Iournol of Oiolaryngology
CONCLUSIONS There was no obvious loss of vestibular nerve fibers or ganglion cells in this patient. The observed changes suggest a pathologic process affecting the vestibular nerve, but they can also be physiologic or due to aging or artifacts. Why, then, did temporary symptomatic imp r o v e m e n t follow the endolyraphatic shunt procedures? A sham effect or biochemical endolymphatic changes as a result of traumatic labyrinthitis have b e e n previously suggested by Schuknecht. 2s The failure of the shunt procedures to alleviate this patient's symptoms perm a n e n t l y was due mainly to the absence of endolymphatic hydrops. It is conceivable that the endolymphatic systems in m a n y patients with Meniere's disease undergoing endolymphatic sac surgery s h o w no endolymphatic bydrops. On the other hand, symptomatic relief of dizziness fol]owing vestibular n e u r e c t o m y might indicate a peripheral site (end organs or first order neuron) of vestibular disease in this case. Such an operation achieved two goals: first, complete denervation of the vestibular end organs and, second, degeneration of the first order neuron of the vestibular system. A more difficult s y m p t o m to explain in this case is the fluctuant hearing loss. No histopathologic findings in the cochlea or in the cochlear nerve of the involved ear explain it. The degree of atrophy of the sensorineural structures in the cochlea was about the same in the t w o ears. At present we have no adequate explanation for the d o c u m e n t e d fluctuations in hearing thresholds. Changes in the endoneurial pressure of the cochlear nerve caused b y chronic compression within the internal auditory canal are a possibility. The authors believe that the findings in the case presented demonstrate that as knowledge of the inner ear increases, the more specific etiologies of the s y m p t o m c o m p l e x of Meniere's disease will be k n o w n and, consequently, the diagnosis of Meniere's disease will be made less frequently.
4. 5. 6. 7. 8. 9.
10. 11, 12. 13. 14. 15. 16.
17. 18. 19. 20. 21. 22.
23. 24.
References
25.
1. Alfaro, V. R.: Diagnostic significance of fullness in the ear. ). Am. Mad. Assoc., 166:329, 1958. 2. House, W. F.: Cryosurgtcal treatment of Meniere's disease. Arch. Otolaryngol., 84:616-629, 1966. 3. Alford, B. R.: Meniere's disease: criteria for diagnosis and evaluation of therapy for reporting. Trans. Am.
284
Acad. Ophthalmol. Otolaryngol., 76:1462-1464, 1972. Belal, A., and House, W. F.: Histopathology of endolymphatic subarachnoid shunt surgery for Meniere's disease. Am. ]. Otoh, 1:37-44, 1979. Belal, A,, Linflficum, F. H., Jr., and House, W. F.: Middle fosse vestibular nerve section: a histopathological report. Am. J. Otol., 1'.72-79, 1979. Klockhoff, I., and Lindblom, U.: Endolymphatic hydrops revealed by glycerol test. Acta Otolaryngol., 61:459-462, 1966. Thomsen, l., and Vesterhauge, g.: A critical evaluation of the glycerol test in Meniare's disease. J. Otolaryngol., 8:145-150, 1979. Belal, A. A., and Antunez, ]. C.: Pathology of endolymphatic hydrops, tin press, 1979.) Schuknecht, H, F.: Endolymphatic hydrops. In Proceedings of the Shambaugh Fifth International Workshop on Middle Ear Microsurgery and Fluctuant Hearing Loss. Huntsville, Alabama, Strode Publishers, Inc., 1977, pp. 371-373. Schuknecht, H. F.: Personal communication. Schuknecht, H. F.: Pathology of the Ear. Cambridge, Harvard University Press, 1974, Belal, A., House, W. F., and Antunez, I, C.: Histopathelegy of cryosurgery for Meniere's disease. Am. J. Otol., 1:147-15(I, 1980. Lindsay, J, R., and Hernenway, W.: Postural vertigo due to unilateral sudden partial loss of vestibular function. Ann. Otol. Rhinoh Laryngol., 65:692-706, 1956. Perlman, H. B., Kirnura, R., and Fernandez, C.: Experiments on temporary obstruction of the internal auditory artery. Laryngoscope, 69:591-613, 1959. Belal, A,: Effects of vascular occlusion on the human inner ear. J. Laryngol, Otol., 93:955-968, 1979. Sando, I., and Egarnl, T.: Inner ear hemorrhage and endolymphatic hydrops in a leukemic patient w i t h sudden hearing loss. Ann. Otol, Rhinol. Laryngol,, 86:518-524, 1977. Ylikosld, J., Collan, Y., and Palva, T.: Pathologic features of the cochlear nerve in profound deafness. Arch. Otolaryngol., 104:202-207, 1978. Co[lan, Y., Ylikoski, J., Palva, T., and Selamaa, R.: Artifacts in eighth cranial nerve biopsy. Acta Otolaryngol. (Stockh.), 89:71-75, 1980. Cragg, B. G., and Thomas, P. K.: The conduction of velocity of regenerated peripheral nerve fibres. I. Physiol. [London), 171:164-175, 1964. Sunderland, S.: The nerve lesion in the carpal b.mnel syndrome. J. Neurol, Neurosurg. Psychiatry, 39:615626, 1976. Fullerton, P. M., end Cilliatt, R. W.: Pressure neuropathy in the hind foot of the guinea pig. J. Neuroh Neurosurg. Psychiatry, 30:18-25, 1067. Andersen, M. H., Fullerton, P. M.,.Gilliatt, R. W., and Hem, J. E. C.: Changes in the forearm associated with median nerve compression at the wrist in the guinea pig. J. Neuro]. Neurosurg. Psychiatry, 33:70-79, 1970. Porter, E. L., and Wharton, P. S.: Irritability of mammalian nerve following ischemia. I. NeurophysioI., 12 '.109-116, 1949. Ylikoski, ]., and House, W. F.'. Morphological findings in the vestibular nerve from patients with vestibular neuritis. (In press.) Schuknecht, H. F.: Pathology of Meniere's disease as it relates to the sac and tack procedures. Ann. Otol. P,hinol. Laryngol., 86:677--682, 1977. Ear Research Institute 256 South Lake Street Los Angeles, California 90057 (Dr. Belal)
PATHOLOGIC SIGNIFICANCE OF MENIERE'S SYMPTOM COMPLEX
Histologic and ultrastructural findings in the temporal bones cf a patient clinically diagnosed as having unilateral Meniere's disease are presented. The patient underwent two endolymphatic subarachnoid shunt operations that failed to relieve symptoms and a middle fossa vestibular nerve section that completely relieved episodic vertigo and stabilized hearing in the ear operated upon. Histopathologic examination of the temporal bones shewed no endolymphatic hydrops in either ear, The maculae and cristae on the side operated upon showed severe degenerative changes attributed to vestibular neurectomy. The cochleograms of the operated and contralateral ears showed degeneration of the sensorineural structures in the basa~ two turns of the cochlea. No apparent cause for the fluctuant hearing loss was found in the cochlea or the cochlear nerve of the involved ear, Light and electron microscopic studies of the vestibular nerve excised at the time of vestibular neurectomy showed that most of the nerve fibers and ganglion cells were essentially normal. Collagen tissue deposition was increased in some areas of the endoneurial space. Most myelinated nerve fibers in these areas had degenerated. Although these changes may be partly due to artifacts and partly due to aging, they probably are the result of a pathologic process affecting the vestibular nerve, These findings suggest that a revised approach to the etiology, pathogenesis, and treatment of Meniere's symptom complex is indicated_
Meniere's disease is characterized by vertiginous episodes, hearing loss, and tinnitus. Alfaro' added fullness and pressure sensation to this symptom complex. The vertiginous episodes usually have a sudden onset, reach maximal intensity within a few minutes, last for an hour or more, and either subside completely or continue as a sensation of imbalance for hours or days. The hearing loss is sensorineural and is characterized by loudness recruitment and decreased speech discrimination scores. There are
fluctuations in hearing, usually for the low frequencies. Tinnitusmay be paroxysmal or constant, varied in pitch and intensity, and increased in severity just before the onset of the vertiginous attack. In the typical attack, pressure sensation and cochlear symptoms precede vertigo. This characteristic presentation of Meniere's disease is not always seen in clinical practice, primarily because of two factors. First, there are atypical forms of Meniere's disease. The each-
Accepted for publication March 26, 1980. *Assistant Professor of Otolaryngology, Alexandria Medicnl School, Alexandria, Egypt. Research Fellow, Ear Itesearch Institute, Los Angeles, California. tAssociatc Professor of Otoloryngology. University of Helsinki,.Helsinki, Finland. Visiting Professor, Ear Research Institute. Los Angeles, California. American Journal of Otolaryngology --Volume 1, Number 4, August 1980
275
American Journal of Otolaryngology
lear form is characterized by fluctuating hearing loss, tinnitus, a n d pressure, b u t no vertigo. Vestibular Meniere's disease p r o d u c e s vertigo, tinnitus, and pressure, but no hearing loss. In Lermoyez's syndrome, fluctuations in hearing occur in reverse relationship to the vertiginous episode; i.e., hearing is i m p r o v e d during and immediately after the attack. In Tumarkin's attacks, the patient experiences an abrupt falling sensation of fleeting duration. Second, two clinical forms, the compensated and u n c o m p e n s a t e d , ensue during the natural course of Meniere's disease. ~ In the compensated form, the vertiginous attack is preceded by increased pressure sensation, tinnitus, and hearing loss. As the frequency of the attacks increases, they u s u a l l y become shorter and occur with fewer warning signs. The pure tone levels tend to drop, a n d speech discrimination does not completely return b e t w e e n attacks. During the decompensated form of the disease, the hearing in the involved ear drops and tinnitus and ear discomfort are continuous. Vertiginous attacks usually occur without warning. The presence of t w o or more diseases complicates the clinical picture even more. Presbycusis and noise i n d u c e d hearing loss are frequently associated with Meniere's disease or other causes of vertigo. This article reports the histopathologic findings in a patient with typical signs and symptoms of Meniere's disease as defined by the Subcommittee on Hearing a n d Equilibrium of the American A c a d e m y of Ophthalmology and Otolaryngology. 3 The clinical diagnosis was unilateral Meniere's disease. The patient underwent two endolympllatic subarachnoid shunt procedures that were unsuccessful in alleviating symptoms and a successful middle fosse vestibular nerve section. Histologic examination of the temporal bones and electron microscopic examination of the vestibular nerves excised at surgery failed to s h o w the cause of the symptoms. The histopathologic findings relating to the endolymphatic subarachnoid shunt operations and vestibular n e u r e c t o m y have been previously reported.4, s
METHODS
AND
MATERIALS
A 62 year old w o m a n was first examined at the Otologic Medical Group, Inc., in May 1971. She had had attacks of dizziness for at least six years. The first attack w a s violent, associated with 276
nausea and vomiting, and persisted for a few days. Attacks occurred every few months. She had fluctuant hearing loss that was more prominent in the right ear than in the left. She also complained of fullness and constant tinnitus of fluctuating intensity in the right ear. Physical examination revealed intact mobile tympanic membranes. The Weber test revealed lateralization to the left ear. There was a 45 dB. average hearing loss with 88 per cent speech discrimination scores in the right ear and a 40 dB. average hearing loss and 92 per cent discrimination scores in the left. B6k6sy tracings and the short increment sensitivity index were compatible with a cochlear lesion in the right ear. Radiographic examination showed normal internal auditory canals bilaterally. Caloric testing with electronystagmography demonstrated directional preponderance to the left. The fluorescent treponemal antibody absorption test was negative. The five hour glucose tolerance test showed a flat curve. A thyroid profile was normal. A diagnosis of right Meniere's disease was made. A vasodilator regimen composed of intravenous doses of histamine, niacin, and'sublingual and subcutaneous doses of histamine was prescribed, b u t the patient continued to be dizzy. A right endolymphatic subarachnoid shunt operation was performed in July 1971. With the patient under general anesthesia, a long silicone rubber shunt tube was inserted between a large, well developed endolymphatic sac and the subarachnoid space. After surgery, dizziness lessened, tinnitus worsened, and hearing levels remained about the same. One year postoperatively spinning attacks recurred. In October 1972 a revision right endolymphatic subarachnoid shunt operation was done with the patient under local anesthesia. The shunt tube, found closed in the endolymphatic sac area, was replaced by another tube that allowed good flow of cerebrospinal fluid. The patient remained free of symptoms for one year, after which she reverted to a pattern of frequent dizzy spells, nausea, and vomiting. Hearing levels in the right ear fluctuated from 48 to 55 dB. average loss. Speech discrimination scores fluctuated b e t w e e n 76 and 92 per cent. In December 1973 a right middle fassa vestibular nerve section was done. With the patient under general anesthesia, the internal auditory canal was exposed by removing bone over the geniculate ganglion and superior semicircular canal. The facial nerve canal was followed and the internal auditory canal opened. The macroscopic appearance of the compartments of the inter-
PATHOLOGIC SIGNIFICANCE OF MENIERE'S SYMPTOMCOMPLEX
hal auditory canal was normal. The superior and inferior vestibular nerves were identified and sectioned separate]y proximal to Scarpa's ganglion, and the distal segments of the nerves were removed. These specimens were immediately fixed in cold 3 per cent Karnovsky's solution overnight, postfixed in 1 per cent osmium tetroxide, processed by alcohol dehydration, and embedded in Epon. One micron thick sections were stained with toluidine blue 0 for light microscopy and thin sections with uranyl acetate and lead citrate for electron microscopy. Postoperatively the patient had mild facial weakness that completely resolved during the next two months. Dryness of the right eye required a tarsorrhaphy. The dizzy spells were completely relieved, although she had some unsteadiness when arising or walking. Tinnitus improved. Audiometric testing, repeated two and eight months postoperatively, showed a 10 dB. improvement in the low tones. Retesting 20 months postoperatively showed regression of auditory function to the preoperative level.
h~ June 1976 the patient died at age 67 of unrelated causes. The autopsy report was not available, and the death-autospy period is unknown. Both temporal bones were acquired at autopsy, fixed in formaldehyde, dehydrated, embedded in celloidin, and sectioned at 20 microns' thickness. Each tenth section was stained with hematoxylin and eosin.
Volume 1 Number 4 August 1780
HISTOPATHOLOGIC FINDINGS The right temporal bone s h o w e d an intact middle ear, tympanic membrane, and ossicles. Bone debris embedded in fibrous tissue was seen in the region of the stapes. The mastoid bone was well pneumatized and showed an operative cavity lined with fibrous tissue. Although the endothelial lining of the endolymphatic sac was identified, the continuity b e t w e e n the area occupied by the flange of the shunt tube and the lining of the sac could not be followed. However, there was minimal fibrosis in the shunt area.
Figure 1. Right temporal bone in which the middle fossa vestibular nerve section had b e e n performed. The superior vestibular nerve was sectioned. The vartleal bony bar (Bill's bar) is the landmark serving to separate the superior vestibular nerve from the facial nerve. The utricle is denervated, and bone formation has occurred i n the lateral semicircular canal.
AZIZ BELAL, JR., AND JUKKA YLIKOSKI
27 7
American
Journa] of Otolaryngology
Figure 2. Rtght temporal bone in w h i c h the middle fossa vestibular nerve section had been performed, The inferior vestibular nerve was sectioned. The saccule is denervated and collapsed. There is herniation of Reissner's membrane in the h o o k region of the cochlear duct into the vestibule where it lies in contact with t h e footplate of the stapes. Bone dust in the region of the stapes was presumably the result of e n d o l y m p h a t i c shunt operations.
Figure 3.
278
Apical coil of the r i g h t cochlea showing a slight outward displacement of Reissner's membrane,
PATHOLOGIC SIGNIFICANCE OF MENIERE'S SYMPTOM COMPLEX
The internal auditory canal showed a surgical defect, which was closed partially by periosteal new hone formation and partially by fibrous tissue. The superior and inferior vestib!flar nerves, presumably excised at the time of vestibular neurectomy, were almost totally replaced by fibrous tissue (Figs. 1, 2). The facial and cochlear nerves appeared to be intact. Few Scarpa's ganglion cells could be identified in the internal auditory canal. The geniculate ganglion and the greater superficial petrosal nerve appeared to be normal. The superior and lateral semicircular canals were filled with fibrous and osteoid tissue that almost completely obliterated their lnmina. The ampullae and neuroepithe[ia of the cristae in both canals were denervated. The maculae of the utricle and saccule were also denervated, but the hair cells appeared to be intact. The saccular walls were collapsed over the macula. Although the posterior ampullary nerve was totally degenerated, the crista of the posterior semicircular
canal appeared normal and showed a basophilic deposit over the cupula. The facial nerve appeared to be normal throughout its course. The cochlear duct shewed no endolymphatic hydrops (Fig. 3). Reissner's membrane showed mild displacement outward in the apical coil. There was herniation of Reissner's membrane in the hook region of the cochlea into the vestibule, where it contacted the undersurface of the footplate of the stapes. Cochlear reconstruction showed severe degeneration in the sensorineural structures in the basal 30 millimeters o f the cochlear duct (Fig. 4). The stria vascularis was normal throughout the cochlear duct. The left temporal bone showed an essentially normal middle ear and mastoid. The internal auditory canal showed intact vestibular, facial, and cochlear nerves. The semicircular canal cristae, as well as the maculae of the utric]e and saccule, had normal innervation. The cochlear duct shewed no endolymphatic hydrops, but
o |174
e
~
99
_'=SX'.'. ~
::+_l~'.( .;wp .,.~leeeefe ,
o
ENDORGANS
O~OqI 9
9 .o/|
L
~
o o otdW-
~
,
o\.~
~
.\.,~
.
Ho,
- }~ _'L82 ?I'"
"X::. :):::
m ~
.
sac
~,~..~,._.~...;l else, w / e e l
/
,
~.
August 1980
VESTI BU t A R
'='",~" Q
9O |
Volume 1 Number 4
./..o
.
.
.
s.p
,o,,
0.
. uJ~eo o/_eoo
ooo\. ,':*ks "+"--~" ",.~o=i- j.,NEURONS ~oo\o ', " | 1 7 6 1 7 6 1 7 6 . . . . . . . . . . ~,'-~o ooo\e
",
u u u _-~ _ o o o~'~
~
Figure 4. Right audiogram and cochleograms showing severe degeneration of the sensorineural structures, more manifest in the basal 10 r a m , of the cochlear duct. The stria vascularis appeared normal throughout. All the vestibular end organs, with the exception of the posterior canal ampulla, showed severe degenerative changes.
o
---'"
_
o ~ ooo
5 o~o(
~
Riqht Ear
o
79,~/ooo
HAIR CELLS
~176
| Intact O Absent
%
Frequency In Cycles Per Second
Atrooh~, __
O R G A N OF CORTI
10
SPIRAL GANGLION ,, , , ,
"'
'
~oS~ r--- O-,- 0-~ --!~!/01 ~a
11O;o
7s !
2S i!i!!i!ii!iiiii
75 sea
1ooo 2ooo 4ooo
~ooo
.....
!i!!iiiiiili;iii!i!',!iii,ililill iiiii,
B0
100 +o
.._....1.:<,.
25
I ~3
STRIA VASCULARIS
Normal .L 10
I 20
30
rnm Cochlear D u c t
AZIZ BELAL, JR., AND JUKKA YLIKOSKI
279
Under electron microscopy the majority of the ~,yeli~:atg~,t r_erve ~bers else a;;peared tc ~e normal. Fibers showing total or partial denudation Df the myelin sheath or bizarre disarrangement of myelin were often located among normal nerve fibers (Fig. 7). Irt some areas there was an apparent increase in the endoneurial connective tissue, in w h i c h case myelin sheaths of remaining nerve fibers were severely fragmented and deformed (Fig. 8). The thickness of the myelin sheaths varied considerably; several had only tO to 15 lamellae. All the vestibular ganglion cells were unmyelinated. They appeared Lo be normal except for several lipofuscin inclusions in the cytoplasm (Fig. 9).
there was slight outward displacement of Reissr_er's membrar, e in tke apica ~-co;,[. Cock!ca: reconstruction showed degeneration of the hair cells from the base to the apex and spiral ganglion atrophy in the basal two turns of the cochlea (Fig. 5). The stria vascularis was normal throughout the cochlear duct. Under light microscopy the majority of the myelinated nerve fibers of the vestibular nerve appeared to be normal. The diameters of individual fibers ranged from 1 to 10 microns. Some groups of fibers s h o w e d relatively small diameters. The myelin sheath was deformed in about 20 per cent of the fibers, particularly those lying in the peripheral areas of the nerve. These fibers appeared as swollen, disorganized, dark material completely I~lling the axis cylinder. The appearance of the vestibular ganglion cells was normal. The amount of endoneurial collagen tissue appeared to be increased .both in the ganglion and in the peripheral zones of the nerve (Fig. 6).
American
Journa! of OtolaryngoJegy
9 e 0/~@
O|
9 ~ooe o\ooe
o oo.,,~
OOOlO Ooole |174o le c o o l e 9 o O l e o o Q I= e o o~.^~lT,,
,,~
o~.ooe
..~.~|
,,\ooo
J ~ - " ~ o N
/'/
l:1
_
f.:!
o o o~,bt e o \ o
| o
e~o0|
m ~ , ~ ~ee
= ,, o p o |
NEURONS
This report raises more questions than it provides answers. The absence of histologic proof of endolymphatic hydrops in a case clinically d[ag-
O~OOe
99 o/a 9 9 o/o
@ Q 0/O
DISCUSSION
~2
0 O 0 "%0 -j ~ ~ V
e%ooe eloeo otoee
"~,~"~_
~-~,.
"**~Z ~.~.ZIu
~
e\ooe
25.~ ~ , ~
~
,,~ujooe
"J~'~'Wl~. O
'~e-boe
~ u ~ / ~
-- I-'~'
Figure 5. Left audiogram a n d cochleogrems showing severe degeneration of the sensorineural structures throughout the cochlear duct. The stria vascularis appeared normal throughout the cochlea.
OAbsent
Left
Ear
Frequency In Cycles Per Second
% Atrophy
ORGAN OF CORTI
75 25 ,o
-
_,
so 1
r'-
vs
SPIRAL GANGLION
iii!!{iiiiliiiiiii;ii!iiii ;ii........
60
70
Discriminalion 9 2 ~
so
250
1
500
1000
I
2000 4 0 0 0
STRIA VASCUL ARIS
8000
751 25 0
280
Normal 10
20
mm Cochlear Duct
30
PATHOLOGIC SIGNIFICANCE a t ;' MENIERE'S SYMPTOM COMPLEX
Volume 1 Number 4
August 19B0
Transversesection of vestibular nerve at the level of Scarpa's ganglion shows several ganglion cells and myelinated nerve fibers. The nerve fibersand ganglion cells appear normal, but the amount of endoneurial connective tissue appears increased. [Epoxyembeddedsection. Toluidine blue 0 stain, x350.)
Figure {3.
nosed as Meniere's disease makes the diagnosis questionable. Episodic vertigo with fiuctuant hearing loss, tinnitus, and pressure sensation made this diagnosis inevitable. With no reliable clinical test for endolymphatic hydrops, misdiagnosis and overdiagnosis of Meniere's disease will continue. Klockhoff and Lindblom 6 reported on the glycerol test as a means of diagnosing endolymphatic hydrops. A positive result indicates Meniere's disease; a negative result does not exclude this diagnosis. However, it has recently been shown that psychologic factors play a significant role in the outcome of this testJ Endolymphatic hydrops is not specific for Meniere's disease. In a recent study, endoiymphatic h y d r o p s was found in 9 per cent of 703 temporal bones available in the temporal bone collection of the Ear Research Institute, Los Angeles. s Included were normal ears of two newborns, poststapedectomy ears, and ears from AZIZ BELAL.JR., AND IUKKAYLIKOSKI
patients with the primary diagnosis of Meniere's disease, Paget's disease, hereditary sensorineural hearing loss, congenital syphilis, and chronic otitis media. Only one-third of these patients had exhibited the typical Meniere s y m p t o m complex, i.e., fluctuant hearing loss, episodic vertigo, tinnitus, and pressure in the ear. How, then, can we explain the Meniere symptom complex in the case presented here? If this case was indeed Meniere's disease, can pressure variations in the e n d o l y m p h occur without displacement of Reissner's membrane and of the saccular membranous walls? The membranous walls of the pars superior, i.e., utric]e and semicircular canals, are k n o w n to be less prone to distention in endolymphatic bydrops than the rest of the membranous labyrinth, although the wails have the same histolog~c structure2 Can the degree of elasticity of these membranes vary from one individual to the next, and, accordingly, can histologic manifestations 281
~meFicGrl
Journol of Otolarynsolosy
Figure 7. Low magnification electron micrograph of vestibular nerve.The majority of myelinatedfibers appear normal Som~ nervefibers are swoIlertandhave deformed,disorganized myelin [arrows). [x3600.)
of endalymphatic hydrops vary? In the case presented, outward displacement of Reissner's membrane in the apical coil of the cochlea in both ears as well as herniation of this membrane in the hook region of the operated ear axe histologic t]ndings that were previously recorded in normal temporal bones.U~ If this case was truly Meniere's disease, it is also possible thai the temporal bones reflected spontaneous remission of the disease, or that the shunt procedures and vestibular neurectomy had relieved the increased endolymphatic pressure. However, it has been previously shown both in animal experiments and in h u m a n temporal bone studies that the membranous wails of the labyrinth behave like varicose veins: once dilated, always dilated. TM "-' Now let us suppose that the case is not Meniere's disease. Disease involving the labyrinth cannot be excluded in this case because of the severe degenerative changes, presumably following vestibular neurectomy. These changes were localized mainly to the superior and lateral
282
An area of increased fibrosis in which the endoneurial space shows depositions of eollagenous material. Myetinated nerve fibers in this area show disintegration of their myelin sheaths. (• 3600.]
Figure 8.
semicircular canals. Although the posterior semicircular canal was similarly denervated, its crista appeared to be normal. The distribution of these degenerative changes in the vestibular system foll~ws the distribution of the anterior vestibular artery, which is presumably cut during vestibular neurectomy. LaPerlman et al. j4 showed t h a t occlusion of the internal auditory artery in guinea pigs produced progressive fibrosis and ossification of the labyrinthine spaces. Similar changes were described in h u m a n temporal bones, presumably following occlusion of the labyrinthine blood vessels. L'~,u~ On the other hand, the myelinated nerve fibers of the vestibular nerve in the biopsy specimen showed changes similar to those reported earlier in h u m a n eighth nerve operative specimens from patients with various ear disorders. ~7 T h e deformation of the myelin sheaths, "hyperplastic myelin," is probably caused by compression during specimen handling, and thus probably is an artifact, is Fragmentation of myelin sheaths often seen in areas with increased fibrosis might
PATHOLOGIC SIGNIFICANCEOF MENIERE'S SYMPTOMCOMPLEX
be a pathologic change. Similarly, the relatively abundant, small caliber, thinly myelinated nerve fibers indicate a stage of regeneration of the nerve. ~ Furthermore, in many neuropathies the loss of nerve fibers and subsequently increased endoneurial fibrosis may be only mild. A typical example of such a change is mild chronic compressive neuropathy. Experimental studies of the peripheral nerves have shown that chronic compression causes congestion of the nerve, which further leads to stasis of endoneurial capillaries, damage to capillary endothelial cells due to hypoxia, and leaking of proteins into the endoneurial space, causing swelling. These conditions in turn lead to stimulation of fibroblastic activity and ultimately to increased fibrosis. TM Simultaneously some of the nerve fibers become affected by increased endoneurial pressure, which is histologically characterized by thinning of nerve fibers, segmental demyelination, wallerian degeneration, and other evidence of
regeneration2'."" These changes are accompanied by physiologic alterations. W h e n nerve fibers become hypoxic, at a certain point they become hyperexcitable and begin to discharge spontaneously. '-'a Increased endoneurial fibrosis combined with regenerative changes in vestibular nerves from patients with vertigo of u n k n o w n etiology has recently been observed2 ~ Because m a n y of these patients also had a narrow internal auditory canal or a .space occupying anatomic structure in the canal, the possibility of chronic compression as the etiologic factor in these cases was suggested. In the case presented, the internal auditory canal was radiologically normal, and the compression theory is thus not directly applicable. However, the compression may have been exerted by blood vessels or arachnoid membranes within the internal auditory canal, or the bony narrowing may have occurred only in the most distal part of the canal, in the cribrose area.
Volume 1 Number 4 August 1980
Figure 9. Two culls of Scarpa's ganglion with numerous lipofuscin inclusions in the peripheral cytoplasm [arrows). The cell on the left shews slightly more filamentous elements in the cytoplasm than the cell an the right. Both cells are surrounded by a thin rim of satellite cell cytoplasm (SI with no myelin sheath. N, nucleus (•
AZIZ BELAL,
IR., AND IUKKA YLIKOSKI
283
Arnericun
.Iournol of Oiolaryngology
CONCLUSIONS There was no obvious loss of vestibular nerve fibers or ganglion cells in this patient. The observed changes suggest a pathologic process affecting the vestibular nerve, but they can also be physiologic or due to aging or artifacts. Why, then, did temporary symptomatic imp r o v e m e n t follow the endolyraphatic shunt procedures? A sham effect or biochemical endolymphatic changes as a result of traumatic labyrinthitis have b e e n previously suggested by Schuknecht. 2s The failure of the shunt procedures to alleviate this patient's symptoms perm a n e n t l y was due mainly to the absence of endolymphatic hydrops. It is conceivable that the endolymphatic systems in m a n y patients with Meniere's disease undergoing endolymphatic sac surgery s h o w no endolymphatic bydrops. On the other hand, symptomatic relief of dizziness fol]owing vestibular n e u r e c t o m y might indicate a peripheral site (end organs or first order neuron) of vestibular disease in this case. Such an operation achieved two goals: first, complete denervation of the vestibular end organs and, second, degeneration of the first order neuron of the vestibular system. A more difficult s y m p t o m to explain in this case is the fluctuant hearing loss. No histopathologic findings in the cochlea or in the cochlear nerve of the involved ear explain it. The degree of atrophy of the sensorineural structures in the cochlea was about the same in the t w o ears. At present we have no adequate explanation for the d o c u m e n t e d fluctuations in hearing thresholds. Changes in the endoneurial pressure of the cochlear nerve caused b y chronic compression within the internal auditory canal are a possibility. The authors believe that the findings in the case presented demonstrate that as knowledge of the inner ear increases, the more specific etiologies of the s y m p t o m c o m p l e x of Meniere's disease will be k n o w n and, consequently, the diagnosis of Meniere's disease will be made less frequently.
4. 5. 6. 7. 8. 9.
10. 11, 12. 13. 14. 15. 16.
17. 18. 19. 20. 21. 22.
23. 24.
References
25.
1. Alfaro, V. R.: Diagnostic significance of fullness in the ear. ). Am. Mad. Assoc., 166:329, 1958. 2. House, W. F.: Cryosurgtcal treatment of Meniere's disease. Arch. Otolaryngol., 84:616-629, 1966. 3. Alford, B. R.: Meniere's disease: criteria for diagnosis and evaluation of therapy for reporting. Trans. Am.
284
Acad. Ophthalmol. Otolaryngol., 76:1462-1464, 1972. Belal, A., and House, W. F.: Histopathology of endolymphatic subarachnoid shunt surgery for Meniere's disease. Am. ]. Otoh, 1:37-44, 1979. Belal, A,, Linflficum, F. H., Jr., and House, W. F.: Middle fosse vestibular nerve section: a histopathological report. Am. J. Otol., 1'.72-79, 1979. Klockhoff, I., and Lindblom, U.: Endolymphatic hydrops revealed by glycerol test. Acta Otolaryngol., 61:459-462, 1966. Thomsen, l., and Vesterhauge, g.: A critical evaluation of the glycerol test in Meniare's disease. J. Otolaryngol., 8:145-150, 1979. Belal, A. A., and Antunez, ]. C.: Pathology of endolymphatic hydrops, tin press, 1979.) Schuknecht, H, F.: Endolymphatic hydrops. In Proceedings of the Shambaugh Fifth International Workshop on Middle Ear Microsurgery and Fluctuant Hearing Loss. Huntsville, Alabama, Strode Publishers, Inc., 1977, pp. 371-373. Schuknecht, H. F.: Personal communication. Schuknecht, H. F.: Pathology of the Ear. Cambridge, Harvard University Press, 1974, Belal, A., House, W. F., and Antunez, I, C.: Histopathelegy of cryosurgery for Meniere's disease. Am. J. Otol., 1:147-15(I, 1980. Lindsay, J, R., and Hernenway, W.: Postural vertigo due to unilateral sudden partial loss of vestibular function. Ann. Otol. Rhinoh Laryngol., 65:692-706, 1956. Perlman, H. B., Kirnura, R., and Fernandez, C.: Experiments on temporary obstruction of the internal auditory artery. Laryngoscope, 69:591-613, 1959. Belal, A,: Effects of vascular occlusion on the human inner ear. J. Laryngol, Otol., 93:955-968, 1979. Sando, I., and Egarnl, T.: Inner ear hemorrhage and endolymphatic hydrops in a leukemic patient w i t h sudden hearing loss. Ann. Otol, Rhinol. Laryngol,, 86:518-524, 1977. Ylikosld, J., Collan, Y., and Palva, T.: Pathologic features of the cochlear nerve in profound deafness. Arch. Otolaryngol., 104:202-207, 1978. Co[lan, Y., Ylikoski, J., Palva, T., and Selamaa, R.: Artifacts in eighth cranial nerve biopsy. Acta Otolaryngol. (Stockh.), 89:71-75, 1980. Cragg, B. G., and Thomas, P. K.: The conduction of velocity of regenerated peripheral nerve fibres. I. Physiol. [London), 171:164-175, 1964. Sunderland, S.: The nerve lesion in the carpal b.mnel syndrome. J. Neurol, Neurosurg. Psychiatry, 39:615626, 1976. Fullerton, P. M., end Cilliatt, R. W.: Pressure neuropathy in the hind foot of the guinea pig. J. Neuroh Neurosurg. Psychiatry, 30:18-25, 1067. Andersen, M. H., Fullerton, P. M.,.Gilliatt, R. W., and Hem, J. E. C.: Changes in the forearm associated with median nerve compression at the wrist in the guinea pig. J. Neuro]. Neurosurg. Psychiatry, 33:70-79, 1970. Porter, E. L., and Wharton, P. S.: Irritability of mammalian nerve following ischemia. I. NeurophysioI., 12 '.109-116, 1949. Ylikoski, ]., and House, W. F.'. Morphological findings in the vestibular nerve from patients with vestibular neuritis. (In press.) Schuknecht, H. F.: Pathology of Meniere's disease as it relates to the sac and tack procedures. Ann. Otol. P,hinol. Laryngol., 86:677--682, 1977. Ear Research Institute 256 South Lake Street Los Angeles, California 90057 (Dr. Belal)
PATHOLOGIC SIGNIFICANCE OF MENIERE'S SYMPTOM COMPLEX