Eur Arch Otorhinolaryngol(1991) 248 :209-217
European Archives of
Oto-RhinoLaryngology © Sprmger-Verlag 1991
Blockage of longitudinal flow in endolymphatic hydrops H . F. Schuknecht ~ and A . Riither 2
~Department of Otolaryngology,MassachusettsEye and Ear Infirmary,Boston, Massachusetts, USA 2KlinikumGrosshadern, HNO-Klinikder Ludwig-Maximilians-Universit~it,Munich, Federal Republic of Germany Received June 8, 1990 / Accepted July 16, 1990
Summary. The external shunt operation on the endolymphatic sac is based on the concept that it will drain excess endolymph and thus arrest the progression of endolymphatic hydrops. We performed histological studies on 46 temporal bones from 13 cases of bilateral and 20 cases of unilateral Meniere's disease to evaluate the status of the pathways of longitudinal flow of endolymph to the sac. The endolymphatic ducts were blocked in 8 specimens (17%), the endolymphatic sinuses'in 9 (19.5%), the utricular ducts in 12 (26%), the saccular ducts in 7 (15%), and the ductus reuniens in 27 (59%). These blockages arrested longitudinal flow from both the pars superior and inferior in 21 cases (46%), the pars superior only in 3 (6.5%), and the pars inferior only in 16 (35%). In the 6 ears with all pathways open, 2 were found to have fistulae between the saccules and the perilymphatic spaces, which theoretically results in internal shunting, thus alleviating the need for the external shunt procedure. In the aggregate, therefore, 42 (91%) of 46 ears showed either areas of blockage of longitudinal flow or internal shunts that would theoretically negate the value of external endolymphatic shunt procedures. These temporal bones, however, are from an autopsy population and the severity of pathological changes is probably greater than it would have been at an earlier age when external shunt surgery might have been a therapeutic consideration. Key words: Endolymphatic hydrops - Meniere's disease - Longitudinal flow
numerous research studies, most of which support the supposition that it has a resorptive function and that loss of this function leads to endolymphatic hydrops [4, 7, 9, 10, 14-16]. In 1927, Portmann [11] first proposed the endolymphatic shunt procedure, which apparently was based on Guild's theory of longitudinal flow. His operation preceded by 11 years the first description of endolymphatic hydrops in Meniere's disease in 1938 and by 38 years the demonstration that experimental ablation of the endolymphatic sac in the guinea pig consistently causes endolymphatic hydrops [8]. Since Portmann's first shunt, many thousands of these procedures have been done throughout the world for the purpose of relieving attacks of vertigo, with most reports indicating a success rate of about 70% [18]. While this figure is quite impressive, it is not clear that it is different from what might occur simply as a placebo effect [17]. A factor that strains the credibility of the shunt operation is the improbability that any kind of drainage device will remain open, given the body's propensity for fibrous envelopment of all foreign material [12]. For the shunt operation to function as a site for drainage of excess endolymph, the pathways of longitudinal flow must remain open. The superior pathway drains the utricle and canals (pars superior) via the utricular duct,
• ~ ~ .~ ~ ~
EndolymphatJc /
Utncle \ ~ ~
Sac ~~
~
. Utncular Duct
A L;ochlear Duct
Introduction
Ever since Guild [5] proposed the longitudinal flow concept and Yamakawa [20] and Hallpike and Cairns [6] discovered endolymphatic hydrops in ears with Meniere's disease, the endolymphatic sac has been a suspect causative organ. Consequently, the sac has been the target for Offprint requests to." H.F. Schuknecht, Department of Otolaryn-
gology, MassachusettsEye and Ear Infirmary, 243 Charles Street, Boston, MA 02114, USA
Endolymphat~c Duct
Sinus
Saccular Duct
Fig. l. Sketch showing the pathways of endolymph flow toward the
endolymphatic sac. A superior pathway serves the pars superior (utricle and canals) and an inferiorpathwayserves the pars inferior (cochlea and saccule)
210
H.F. Schuknecht and A. Riither: Endolymphatic flow
Table 1. Histological findings for blockages or fistulae in 46 temporal bones with premortem Meniere's disease Ear
Blockage E duct
Fistulae E sinus
U duct
1
S duct
S
4-
4-
4-
+ 4-
4-
+
6
S-U
4-
4+
C-S
+
4 5
C-P
44-
3
S-P
4-
+
2
DR
4-
7
+
4-
8
+
9
+
4+
10
+
+
11
+
12
+
4-
+
13 14 15 4-
16 17 18 19
+
20 21 23
+
+
22
+
+
+
24 4-
25 4-
26
+
4-
27
+
28 4-
29 30 31 32
4-
33 4-
34
+
4-
35 36 37
4-
38
4-
+ +
39 40
+
+ +
41
+ +
42 +
43
+
44
+ + +
+
+
+
45 46
Totals
8
9
12
7
1
27
9
E, Endolymphatic; U, utricle; S, saccule; DR, ductus reuniens; P, perilymphatic space; C, cochlear duct
1
+
+
7
4
H. F. Schuknecht and A. Rtither: Endolymphatic flow
211
Fig. 2. Ears 7 and 8. Bilateral Meniere's disease, male, age 78. The vestibular aqueducts are filled with a fibrous tissue. The endolymphatic ducts consist of central strands of epithelial cells showing no lumens (arrows). x 306
and the inferior pathway drains the cochlear duct and saccule (pars inferior) via the ductus reuniens, saccule, and saccular duct (Fig. 1). The purpose of the current study was to examine histological preparations of human ears with endolymphatic hydrops and to determine whether alterations in the membranous labyrinths interfere with these pathways of flow.
Materials and methods In the temporal bone collection at the Massachusetts Eye and Ear Infirmary, there are specimens from 33 persons who had clinical histories consistent with Meniere's disease. All cases had histories and audiometric profiles of unilateral or bilateral progressive sensorineural hearing loss with flat threshold patterns. Most of these cases also had documented fluctuations of hearing levels. Three cases failed to have vertigo, although their hearing losses were typical of Meniere's disease. There were an additional 5 cases in which the medical records indicated complaints of constant or intermittent unsteadiness rather than the classical episodic vertigo with nausea and vomiting. In 13 cases (40%), the disease was bilateral and in 20 it was unilateral, which is a similar incidence to that reported for clinical populations [13]. The temporal bones were prepared for light microscopic study by the standard method of fixation, decalcification, embedding in celloidin, serially sectioning in the horizontal plane at a thickness of 20 lam, staining with hematoxylin and eosin, and mounting every tenth section on glass slides. In these studies, we concentrated on the status of the membranes of the labyrinth in terms of distention, ruptures, outpouchings, fistulae, collapse, atrophy and fibrosis.
Results All 46 ears showed severe endolymphatic hydrops. The endolymphatic duct was blocked in 8 (17%) of the 46 ears (Table 1). In 5 of the specimens, all that remained of the ducts was a strand of epithelial cells with no lumen,
which was located in the center of a vestibular aqueduct filled with fibrous tissue (Fig. 2). In both ears of one subject, the ducts were encroached upon and blocked by small fibro-osseous lesions of unknown etiology (Fig. 3). In one case of unilateral endolymphatic hydrops, the duct was blocked by an intracanalicular bone growth of unknown cause (Figs. 4, 5). The lumen of the endolymphatic sinus was bridged by a membrane in 9 (19.5%) of the 46 ears (Figs. 6, 7), all of which were different ears than those with blocked endolymphatic ducts. The origin of this membrane in most cases was either a distended saccular wall or a dilated saccular duct. The utricle did not appear to dilate sufficiently to block the sinus. The utricular duct was blocked in 12 (26%) of the 46 ears. In 6 of these, the cause was compression by an enlarged saccule and/or cochlear duct, 3 showed fibrous blockage of their lumens, 2 had blocked utriculoendolymphatic valves (Fig. 8), and 1 was blocked by a collapsed utricle. The saccular duct was collapsed by pressure from an enlarged saccule or cochlear duct so that no lumen could be found in 7 (15%) of the ears. The ductus reuniens was blocked in 27 (59%) of the 46 ears, and in 16 (35%) of the 46 it was the only area of blockage from the cochlea to the endolymphatic sac (Fig. 9). The most c o m m o n cause for the blocked ductus reuniens was compression by an enlarged saccule. However, in one ear both the ductus reuniens and saccule were totally collapsed, so that no lumens remained (Figs. 10, ii). Six ears showed all pathways to be open (Fig. 12). Two of the 6 had saccular ruptures into the perilymphatic space; 1 case had a history of vertigo, the other did not. Unhealed ruptures (fistulae) were found in the membranous labyrinths of 18 of the 46 ears (39%). As described previously [1], outpouchings were either healed
212
Fig. 3. Ears 11 and 12. Bilateral Meniere's disease, female, age 75. There are small focal areas of bone resorption and new bone formation involving the vestibular aqueducts and posterior semicircular canals in b o t h ears. These views show fibro-osseous proliferation and blockage of the vestibular aqueducts and their contained endolymphatic ducts (arrows). x 36.2 Fig. 4 A , B. E a r 40. Left Meniere's disease, female. This woman complained of fluctuating hearing at the age of 42. A n audiogram
H.F. Schuknecht and A. Rtither: Endolymphatic flow
showed a 5 0 - 7 0 d B sensorineural hearing loss on the left side characterized by a flat threshold pattern and 84% discrimination score. She denied having vertigo or tinnitus. She died of renal failure 5 days later. There is a fibro-osseous obliteration of the vestibular aqueduct in the left ear (arrow). O t h e r sections show a moderately severe hydrops of the cochlear duct, saccule and utricle, and a fistula between the saccule and perilymphatic space of the vestibule, x 16 and x 65
H. F. Schuknecht and A. Rtither: Endolymphatic flow
~'~'*'~;' ~,'"
D~lated Saccule and / Cochlear Duct
ObstructEon of
Endolymphatlc Duct
Fig. 5. Sketch showing blockage of longitudinal flow by a solid
space-occupying lesion of the endolymphatic duct resulting in endolymphatic hydrops.
fistulae or herniations of the outer layer of the membranous wall through a break in the inner layer. However, we have not designated these findings as fistulae (Fig. 13). In 10 of these 18 fistulae, the openings were located between the endolymphatic and perilymphatic spaces; 9 were in the saccular wall and 1 in a herniated cochlear duct. These 10 ears were from 8 persons with unilateral and 1 with bilateral disease.
Discussion The question arises as to whether there is a need for a longitudinal flow system if excess endolymph can
213 drain into the perilymphatic space via a fistula. The cochleosacculotomy operation is based on this concept. Such fistulae would theoretically act as escape routes for accumulating endolymph, which might arrest the progression of endolymphatic hydrops. These fistulae would be useful only if there were open pathways to them. Histological study of the 10 ears with endolymph to perilymph fistulae (9 saccular, 1 cochlear) showed that 6 drained the superior pathway only, 2 drained the inferior pathway only, and 2 drained both pathways. Eight ears had fistulae between two or more endolymphatic spaces (Figs. 14, 15). Seven ears had fistulae between the saccules and cochlear ducts (Figs. 6, 7, 14), of which 3 also were fistulized into the utricles; an additional ear had a fistula between the saccule and utricle only (Fig. 14). These findings are suggestive as to whether fistulae between the endolymphatic spaces could serve as bypasses for longitudinal flow. This did occur in 1 ear in which a fistula between the cochlear duct and saccule allowed the cochlear flow to detour past a blocked ductus reuniens to enter an otherwise open endolymphatic pathway. For external shunt procedures to have any chance of success in controlling hydrops and relieving episodic vertigo, assuming the longitudinal flow concept is valid, the pathways to the endolymphatic sac must remain patent. Among the 46 ears in our present study, 21 (46%) had blockage of both superior and inferior pathways of flow to the endolymphatic sac. An additional 16 (35%) had blockage of the inferior pathway only and 3 (6.5%) had
Fig. 6. Ear 2. Bilateral Meniere's disease, female, age 65, left ear. There is a fistula between the dilated cochlear duct and saccule. A membrane bridges the lumen of the endolymphatic sinus which presumably blocks longitudinal flow. x 13 and × 56
214
A
H.F. Schuknecht and A. Riither: Endolymphatic flow
125 250 i
i
500
IK
i
i
2K
4K
8K
i
i
i
16K i
0
0
IO
I0 20
20
X
30
:50
40
40
50
50
6D
60
7C
70
8G
80
90
90 I00
I00 Discnm. 8 %
I10
I10
HAIR CELLS
COCHLEAR NEURONS
]
STRIA VASCULARIS t 310 APEX
NORMAL 215
210 1'5 I0 DISTANCE IN MM
~)
0 BASE
Fig. 7A, B. Ear 5. Bilateral Meniere's disease, male, age 78, right ear. A large cochlear duct fills the vestibule. The utricle is dilated and the sinus of the endolymphatic duct is blocked by membranes. Other sections show blockage at the ductus reuniens, saccular duct and utricular duct. x 10 and x 43 Fig.8A, B. Ear 16. Right Meniere's disease, female, age 53. A The audiogram made at age 51 shows the typical flat threshold pat-
tern with complete loudness recruitment at 1 kHz. There is a loss of hair cells and neurons limited to the basal end of the cochlea. B An enormously dilatated saccule fills the vestibule and has fistulized into the sinus of the endolymphatic duct. No membranes bridge the lumen of the sinus. It has also caused pressure blockage of the utriculoendolymphatic valve and utricular duct. The endolymph of the utricle and canals shows acidophilic staining, indicating an increased protein content. × 18
H. F. Schuknecht and A. Rtither: Endolymphatic flow
215
D~lated Saccule
Fig. 9A, B. Ear 44. Right Meniere's disease, male, age 74. The ductus reuniens (arrow) is occluded by pressure from a dilated cochlear duct. Other sections show that the saccular duct is also occluded. × 19 and x 105
~"
blockage of the superior pathway only. Fistulae between the endolymphatic and perilymphatic spaces were present in both the superior and inferior pathways in 2 ears. In 4 ears such fistulae were seen in the saccules (inferior pathways) only and in each case cochlear flow was blocked by a collapsed ductus reuniens. In these cases, flow from the superior pathways had access to the fistulae by retrograde flow through patent saccular ducts. A total of 40 (87%) of the 46 ears showed one or m o r e sites of blockage of longitudinal flow. A m o n g the 6 remaining ears having all pathways open, there were 2 with saccular fistulae into the perilymphatic spaces, which theoretically resulted in internal shunting. In the aggregate, therefore, there were 42 ears (91%) of the 46 examined that showed either blocked pathways of longitudinal flow or internal shunts. We do not think that our study is flawed by misinterpretations of p o s t m o r t e m autolytic change or by artifacts of histological preparation. The judgment that a change was pathological was based on comparison with normal ears processed in a similar m a n n e r and, in the case of unilateral Meniere's disease, by comparison with the opposite ear. The average age of our subjects was 70.64 years, whereas the average age of patients seeking medical relief from the symptoms of Meniere's disease is in the range of 40-50 years [2, 3, 19]. It is reasonable to assume, therefore, that the pathological changes are more
~
~ ~ .%-~-~
='~-
B
A
Fig. 10. Sketch demonstrating a large dilated saccule that has caused pressure-occlusion of the ductus reuniens (A), saccular duct (B) and utricular duct (C)
~\~\%~ Z,
Dilated Cochlear Duct
Fig. 11. Sketch depicting a dilated cochlear duct herniated into the vestibule causing collapse of the saccule (A) and pressure occlusion of the utricular duct (B) and ductus reuniens (C)
advanced in our autopsy population than they would have b e e n earlier in life when any symptoms would have been m o r e florid and when external shunt surgery might have been a therapeutic option. We cannot relate further to the question of age than to recognize it as a factor in interpreting the significance of our findings.
216
H.F. Schuknecht and A. Rtither: Endolymphatic flow
12
13 Fig. 12A, B. Ear 13. Left Meniere's disease, male, age 73. In spite of moderately severe dilatation of the membranous labyrinth all pathways of longitudinal flow are open. These views show the dilated utricular and saccular ducts (arrows). A break in the saccular wall is sealed off by fibrous tissue, x 19
Fig. 13. Ear 2. Bilateral Meniere's disease, female, age 65, left ear. A moderately dilated utricle shows an outpouching of wall. It is not clear whether this break in continuity involved only the inner layer with the outer layer undergoing distention, or whether there was a complete rupture followed by regeneration of a thin membrane, x 32.3
H. F. Schuknecht and A. Rtither: Endolymphatic flow
217
Fig. 14. Ears 22 and 23. Bilateral Meniere's disease, female, age 71. In the right ear there is a fistula (arrow) between the saccule and cochlear duct and in the left ear (arrow) between the saccule and utricle. × 13.5
I~
\~
Utrlcle ~
Cochlear Duct
Fig. 15. Schematic view demonstrating endolymphatic fistulae between the cochlear duct, saccule and utricle. It is theoretically possible for fistulae to establish detours by which endolymph can bypass areas of blocked longitudinal flow
Acknowledgement. This study was supported by grant DC 00079 from the National Institute on Deafness and Other Communication Disorders.
References 1. Altmann F, Kornfeld M (1965) Histological studies of Meniere's disease. Ann Otol Rhinol Laryngol 74 : 915-943 2. Brown JS (1983) A ten year statistical follow-up of 245 consecutive cases of endolymphatic shunt and decompression with 328 consecutive cases of labyrinthectomy. Laryngoscope 93: 1419-1424 3. Chui RTK, McCabe BF, Harker LA (1982) Meniere's disease at the University of Iowa: 1973 to 1980. Otolaryngol Head Neck Surg 90: 482-487 4. Engstr6m H, Hjorth S (1951) On the distribution and localization of injected dyes in the labyrinth of the guinea pig. Acta Otolaryngol (Stockh) [Suppl] 95 : 149-158
5. Guild SR (1927) The circulation of the endolymph. Am J Anat 39 : 57-81 6. Hallpike C, Cairns H (1938) Observations on the pathology of Meniere's syndrome. J Laryngol Otol 53 : 625-655 7. Ishii T, Silverstein H, Balogh K Jr (1966) Metabolic activities of the endolymphatic sac. Acta Otolaryngol (Stockh) 62:6173 8. Kimura RS, Schuknecht HF (1965) Membranous hydrops in the inner ear of the guinea pig after obliteration of the endolymphatic sac. Pract Otorhinolaryngol 27 : 343-354 9. Kimura RS, Schuknecht HF, Ota CY, Jones DD (1980) Obliteration of the ductus reuniens. Acta Otolaryngol (Stockh) 89: 295-309 10. Lundquist P-G (1976) Aspects on endolymphatic sac morphology and function. Arch Otorhinolaryngol 212 : 231-240 11. Portmann G (1927) Vertigo. Surgical treatment by opening of the saccus endolymphaticus. Arch Otolaryngol 6:309-315 12. Schuknecht HF (1977) Pathology of Meniere's disease as it relates to the sac and tack procedures. Ann Otol Rhinol Laryngol 86: 677-682 13. Schuknecht HF (1989) Meniere's disease. In: English JM (ed) Otolaryngology. Lippincott, Philadelphia, pp 1-23 14. Schuknecht HF, Seifi AE (1963) Experimental observations on the fluid physiology of the inner ear. Ann Otol Rhinol Laryngol 72 : 687-712 15. Schuknecht HF, Northrop C, Igarashi M (1968) Cochlear pathology after destruction of the endolymphatic sac in the cat. Acta Otolaryngol (Stockh) 65 : 479-487 16. Silverstein H (1966) Biochemical and physiologic studies of the endolymphatic sac in the cat. Laryngoscope 76:498-512 17. Thomsen J, Bretlau P (1986) General conclusions. In: Pfaltz CR (ed) Controversial aspects of Meniere's disease. Thieme, New York, pp 120-136 18. Torok N (1977) Old and new in Meniere's disease. Laryngoscope 87 : 1870-1877 19. Wladislavosky-WasermanP, Facer GW, Mokri B, Kurland LT (1984) Meniere's disease: a 30-year epidemiologic and clinical study in Rochester, MN, 1951-1980. Laryngoscope 94:10981102 20. Yamakawa K (1938) The inner ear of a patient with Meniere's syndrome. J Otorhinolaryngol Soc Jpn 44:2310-2312
European Archives of
Oto-RhinoLaryngology © Sprmger-Verlag 1991
Blockage of longitudinal flow in endolymphatic hydrops H . F. Schuknecht ~ and A . Riither 2
~Department of Otolaryngology,MassachusettsEye and Ear Infirmary,Boston, Massachusetts, USA 2KlinikumGrosshadern, HNO-Klinikder Ludwig-Maximilians-Universit~it,Munich, Federal Republic of Germany Received June 8, 1990 / Accepted July 16, 1990
Summary. The external shunt operation on the endolymphatic sac is based on the concept that it will drain excess endolymph and thus arrest the progression of endolymphatic hydrops. We performed histological studies on 46 temporal bones from 13 cases of bilateral and 20 cases of unilateral Meniere's disease to evaluate the status of the pathways of longitudinal flow of endolymph to the sac. The endolymphatic ducts were blocked in 8 specimens (17%), the endolymphatic sinuses'in 9 (19.5%), the utricular ducts in 12 (26%), the saccular ducts in 7 (15%), and the ductus reuniens in 27 (59%). These blockages arrested longitudinal flow from both the pars superior and inferior in 21 cases (46%), the pars superior only in 3 (6.5%), and the pars inferior only in 16 (35%). In the 6 ears with all pathways open, 2 were found to have fistulae between the saccules and the perilymphatic spaces, which theoretically results in internal shunting, thus alleviating the need for the external shunt procedure. In the aggregate, therefore, 42 (91%) of 46 ears showed either areas of blockage of longitudinal flow or internal shunts that would theoretically negate the value of external endolymphatic shunt procedures. These temporal bones, however, are from an autopsy population and the severity of pathological changes is probably greater than it would have been at an earlier age when external shunt surgery might have been a therapeutic consideration. Key words: Endolymphatic hydrops - Meniere's disease - Longitudinal flow
numerous research studies, most of which support the supposition that it has a resorptive function and that loss of this function leads to endolymphatic hydrops [4, 7, 9, 10, 14-16]. In 1927, Portmann [11] first proposed the endolymphatic shunt procedure, which apparently was based on Guild's theory of longitudinal flow. His operation preceded by 11 years the first description of endolymphatic hydrops in Meniere's disease in 1938 and by 38 years the demonstration that experimental ablation of the endolymphatic sac in the guinea pig consistently causes endolymphatic hydrops [8]. Since Portmann's first shunt, many thousands of these procedures have been done throughout the world for the purpose of relieving attacks of vertigo, with most reports indicating a success rate of about 70% [18]. While this figure is quite impressive, it is not clear that it is different from what might occur simply as a placebo effect [17]. A factor that strains the credibility of the shunt operation is the improbability that any kind of drainage device will remain open, given the body's propensity for fibrous envelopment of all foreign material [12]. For the shunt operation to function as a site for drainage of excess endolymph, the pathways of longitudinal flow must remain open. The superior pathway drains the utricle and canals (pars superior) via the utricular duct,
• ~ ~ .~ ~ ~
EndolymphatJc /
Utncle \ ~ ~
Sac ~~
~
. Utncular Duct
A L;ochlear Duct
Introduction
Ever since Guild [5] proposed the longitudinal flow concept and Yamakawa [20] and Hallpike and Cairns [6] discovered endolymphatic hydrops in ears with Meniere's disease, the endolymphatic sac has been a suspect causative organ. Consequently, the sac has been the target for Offprint requests to." H.F. Schuknecht, Department of Otolaryn-
gology, MassachusettsEye and Ear Infirmary, 243 Charles Street, Boston, MA 02114, USA
Endolymphat~c Duct
Sinus
Saccular Duct
Fig. l. Sketch showing the pathways of endolymph flow toward the
endolymphatic sac. A superior pathway serves the pars superior (utricle and canals) and an inferiorpathwayserves the pars inferior (cochlea and saccule)
210
H.F. Schuknecht and A. Riither: Endolymphatic flow
Table 1. Histological findings for blockages or fistulae in 46 temporal bones with premortem Meniere's disease Ear
Blockage E duct
Fistulae E sinus
U duct
1
S duct
S
4-
4-
4-
+ 4-
4-
+
6
S-U
4-
4+
C-S
+
4 5
C-P
44-
3
S-P
4-
+
2
DR
4-
7
+
4-
8
+
9
+
4+
10
+
+
11
+
12
+
4-
+
13 14 15 4-
16 17 18 19
+
20 21 23
+
+
22
+
+
+
24 4-
25 4-
26
+
4-
27
+
28 4-
29 30 31 32
4-
33 4-
34
+
4-
35 36 37
4-
38
4-
+ +
39 40
+
+ +
41
+ +
42 +
43
+
44
+ + +
+
+
+
45 46
Totals
8
9
12
7
1
27
9
E, Endolymphatic; U, utricle; S, saccule; DR, ductus reuniens; P, perilymphatic space; C, cochlear duct
1
+
+
7
4
H. F. Schuknecht and A. Rtither: Endolymphatic flow
211
Fig. 2. Ears 7 and 8. Bilateral Meniere's disease, male, age 78. The vestibular aqueducts are filled with a fibrous tissue. The endolymphatic ducts consist of central strands of epithelial cells showing no lumens (arrows). x 306
and the inferior pathway drains the cochlear duct and saccule (pars inferior) via the ductus reuniens, saccule, and saccular duct (Fig. 1). The purpose of the current study was to examine histological preparations of human ears with endolymphatic hydrops and to determine whether alterations in the membranous labyrinths interfere with these pathways of flow.
Materials and methods In the temporal bone collection at the Massachusetts Eye and Ear Infirmary, there are specimens from 33 persons who had clinical histories consistent with Meniere's disease. All cases had histories and audiometric profiles of unilateral or bilateral progressive sensorineural hearing loss with flat threshold patterns. Most of these cases also had documented fluctuations of hearing levels. Three cases failed to have vertigo, although their hearing losses were typical of Meniere's disease. There were an additional 5 cases in which the medical records indicated complaints of constant or intermittent unsteadiness rather than the classical episodic vertigo with nausea and vomiting. In 13 cases (40%), the disease was bilateral and in 20 it was unilateral, which is a similar incidence to that reported for clinical populations [13]. The temporal bones were prepared for light microscopic study by the standard method of fixation, decalcification, embedding in celloidin, serially sectioning in the horizontal plane at a thickness of 20 lam, staining with hematoxylin and eosin, and mounting every tenth section on glass slides. In these studies, we concentrated on the status of the membranes of the labyrinth in terms of distention, ruptures, outpouchings, fistulae, collapse, atrophy and fibrosis.
Results All 46 ears showed severe endolymphatic hydrops. The endolymphatic duct was blocked in 8 (17%) of the 46 ears (Table 1). In 5 of the specimens, all that remained of the ducts was a strand of epithelial cells with no lumen,
which was located in the center of a vestibular aqueduct filled with fibrous tissue (Fig. 2). In both ears of one subject, the ducts were encroached upon and blocked by small fibro-osseous lesions of unknown etiology (Fig. 3). In one case of unilateral endolymphatic hydrops, the duct was blocked by an intracanalicular bone growth of unknown cause (Figs. 4, 5). The lumen of the endolymphatic sinus was bridged by a membrane in 9 (19.5%) of the 46 ears (Figs. 6, 7), all of which were different ears than those with blocked endolymphatic ducts. The origin of this membrane in most cases was either a distended saccular wall or a dilated saccular duct. The utricle did not appear to dilate sufficiently to block the sinus. The utricular duct was blocked in 12 (26%) of the 46 ears. In 6 of these, the cause was compression by an enlarged saccule and/or cochlear duct, 3 showed fibrous blockage of their lumens, 2 had blocked utriculoendolymphatic valves (Fig. 8), and 1 was blocked by a collapsed utricle. The saccular duct was collapsed by pressure from an enlarged saccule or cochlear duct so that no lumen could be found in 7 (15%) of the ears. The ductus reuniens was blocked in 27 (59%) of the 46 ears, and in 16 (35%) of the 46 it was the only area of blockage from the cochlea to the endolymphatic sac (Fig. 9). The most c o m m o n cause for the blocked ductus reuniens was compression by an enlarged saccule. However, in one ear both the ductus reuniens and saccule were totally collapsed, so that no lumens remained (Figs. 10, ii). Six ears showed all pathways to be open (Fig. 12). Two of the 6 had saccular ruptures into the perilymphatic space; 1 case had a history of vertigo, the other did not. Unhealed ruptures (fistulae) were found in the membranous labyrinths of 18 of the 46 ears (39%). As described previously [1], outpouchings were either healed
212
Fig. 3. Ears 11 and 12. Bilateral Meniere's disease, female, age 75. There are small focal areas of bone resorption and new bone formation involving the vestibular aqueducts and posterior semicircular canals in b o t h ears. These views show fibro-osseous proliferation and blockage of the vestibular aqueducts and their contained endolymphatic ducts (arrows). x 36.2 Fig. 4 A , B. E a r 40. Left Meniere's disease, female. This woman complained of fluctuating hearing at the age of 42. A n audiogram
H.F. Schuknecht and A. Rtither: Endolymphatic flow
showed a 5 0 - 7 0 d B sensorineural hearing loss on the left side characterized by a flat threshold pattern and 84% discrimination score. She denied having vertigo or tinnitus. She died of renal failure 5 days later. There is a fibro-osseous obliteration of the vestibular aqueduct in the left ear (arrow). O t h e r sections show a moderately severe hydrops of the cochlear duct, saccule and utricle, and a fistula between the saccule and perilymphatic space of the vestibule, x 16 and x 65
H. F. Schuknecht and A. Rtither: Endolymphatic flow
~'~'*'~;' ~,'"
D~lated Saccule and / Cochlear Duct
ObstructEon of
Endolymphatlc Duct
Fig. 5. Sketch showing blockage of longitudinal flow by a solid
space-occupying lesion of the endolymphatic duct resulting in endolymphatic hydrops.
fistulae or herniations of the outer layer of the membranous wall through a break in the inner layer. However, we have not designated these findings as fistulae (Fig. 13). In 10 of these 18 fistulae, the openings were located between the endolymphatic and perilymphatic spaces; 9 were in the saccular wall and 1 in a herniated cochlear duct. These 10 ears were from 8 persons with unilateral and 1 with bilateral disease.
Discussion The question arises as to whether there is a need for a longitudinal flow system if excess endolymph can
213 drain into the perilymphatic space via a fistula. The cochleosacculotomy operation is based on this concept. Such fistulae would theoretically act as escape routes for accumulating endolymph, which might arrest the progression of endolymphatic hydrops. These fistulae would be useful only if there were open pathways to them. Histological study of the 10 ears with endolymph to perilymph fistulae (9 saccular, 1 cochlear) showed that 6 drained the superior pathway only, 2 drained the inferior pathway only, and 2 drained both pathways. Eight ears had fistulae between two or more endolymphatic spaces (Figs. 14, 15). Seven ears had fistulae between the saccules and cochlear ducts (Figs. 6, 7, 14), of which 3 also were fistulized into the utricles; an additional ear had a fistula between the saccule and utricle only (Fig. 14). These findings are suggestive as to whether fistulae between the endolymphatic spaces could serve as bypasses for longitudinal flow. This did occur in 1 ear in which a fistula between the cochlear duct and saccule allowed the cochlear flow to detour past a blocked ductus reuniens to enter an otherwise open endolymphatic pathway. For external shunt procedures to have any chance of success in controlling hydrops and relieving episodic vertigo, assuming the longitudinal flow concept is valid, the pathways to the endolymphatic sac must remain patent. Among the 46 ears in our present study, 21 (46%) had blockage of both superior and inferior pathways of flow to the endolymphatic sac. An additional 16 (35%) had blockage of the inferior pathway only and 3 (6.5%) had
Fig. 6. Ear 2. Bilateral Meniere's disease, female, age 65, left ear. There is a fistula between the dilated cochlear duct and saccule. A membrane bridges the lumen of the endolymphatic sinus which presumably blocks longitudinal flow. x 13 and × 56
214
A
H.F. Schuknecht and A. Riither: Endolymphatic flow
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Fig. 7A, B. Ear 5. Bilateral Meniere's disease, male, age 78, right ear. A large cochlear duct fills the vestibule. The utricle is dilated and the sinus of the endolymphatic duct is blocked by membranes. Other sections show blockage at the ductus reuniens, saccular duct and utricular duct. x 10 and x 43 Fig.8A, B. Ear 16. Right Meniere's disease, female, age 53. A The audiogram made at age 51 shows the typical flat threshold pat-
tern with complete loudness recruitment at 1 kHz. There is a loss of hair cells and neurons limited to the basal end of the cochlea. B An enormously dilatated saccule fills the vestibule and has fistulized into the sinus of the endolymphatic duct. No membranes bridge the lumen of the sinus. It has also caused pressure blockage of the utriculoendolymphatic valve and utricular duct. The endolymph of the utricle and canals shows acidophilic staining, indicating an increased protein content. × 18
H. F. Schuknecht and A. Rtither: Endolymphatic flow
215
D~lated Saccule
Fig. 9A, B. Ear 44. Right Meniere's disease, male, age 74. The ductus reuniens (arrow) is occluded by pressure from a dilated cochlear duct. Other sections show that the saccular duct is also occluded. × 19 and x 105
~"
blockage of the superior pathway only. Fistulae between the endolymphatic and perilymphatic spaces were present in both the superior and inferior pathways in 2 ears. In 4 ears such fistulae were seen in the saccules (inferior pathways) only and in each case cochlear flow was blocked by a collapsed ductus reuniens. In these cases, flow from the superior pathways had access to the fistulae by retrograde flow through patent saccular ducts. A total of 40 (87%) of the 46 ears showed one or m o r e sites of blockage of longitudinal flow. A m o n g the 6 remaining ears having all pathways open, there were 2 with saccular fistulae into the perilymphatic spaces, which theoretically resulted in internal shunting. In the aggregate, therefore, there were 42 ears (91%) of the 46 examined that showed either blocked pathways of longitudinal flow or internal shunts. We do not think that our study is flawed by misinterpretations of p o s t m o r t e m autolytic change or by artifacts of histological preparation. The judgment that a change was pathological was based on comparison with normal ears processed in a similar m a n n e r and, in the case of unilateral Meniere's disease, by comparison with the opposite ear. The average age of our subjects was 70.64 years, whereas the average age of patients seeking medical relief from the symptoms of Meniere's disease is in the range of 40-50 years [2, 3, 19]. It is reasonable to assume, therefore, that the pathological changes are more
~
~ ~ .%-~-~
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A
Fig. 10. Sketch demonstrating a large dilated saccule that has caused pressure-occlusion of the ductus reuniens (A), saccular duct (B) and utricular duct (C)
~\~\%~ Z,
Dilated Cochlear Duct
Fig. 11. Sketch depicting a dilated cochlear duct herniated into the vestibule causing collapse of the saccule (A) and pressure occlusion of the utricular duct (B) and ductus reuniens (C)
advanced in our autopsy population than they would have b e e n earlier in life when any symptoms would have been m o r e florid and when external shunt surgery might have been a therapeutic option. We cannot relate further to the question of age than to recognize it as a factor in interpreting the significance of our findings.
216
H.F. Schuknecht and A. Rtither: Endolymphatic flow
12
13 Fig. 12A, B. Ear 13. Left Meniere's disease, male, age 73. In spite of moderately severe dilatation of the membranous labyrinth all pathways of longitudinal flow are open. These views show the dilated utricular and saccular ducts (arrows). A break in the saccular wall is sealed off by fibrous tissue, x 19
Fig. 13. Ear 2. Bilateral Meniere's disease, female, age 65, left ear. A moderately dilated utricle shows an outpouching of wall. It is not clear whether this break in continuity involved only the inner layer with the outer layer undergoing distention, or whether there was a complete rupture followed by regeneration of a thin membrane, x 32.3
H. F. Schuknecht and A. Rtither: Endolymphatic flow
217
Fig. 14. Ears 22 and 23. Bilateral Meniere's disease, female, age 71. In the right ear there is a fistula (arrow) between the saccule and cochlear duct and in the left ear (arrow) between the saccule and utricle. × 13.5
I~
\~
Utrlcle ~
Cochlear Duct
Fig. 15. Schematic view demonstrating endolymphatic fistulae between the cochlear duct, saccule and utricle. It is theoretically possible for fistulae to establish detours by which endolymph can bypass areas of blocked longitudinal flow
Acknowledgement. This study was supported by grant DC 00079 from the National Institute on Deafness and Other Communication Disorders.
References 1. Altmann F, Kornfeld M (1965) Histological studies of Meniere's disease. Ann Otol Rhinol Laryngol 74 : 915-943 2. Brown JS (1983) A ten year statistical follow-up of 245 consecutive cases of endolymphatic shunt and decompression with 328 consecutive cases of labyrinthectomy. Laryngoscope 93: 1419-1424 3. Chui RTK, McCabe BF, Harker LA (1982) Meniere's disease at the University of Iowa: 1973 to 1980. Otolaryngol Head Neck Surg 90: 482-487 4. Engstr6m H, Hjorth S (1951) On the distribution and localization of injected dyes in the labyrinth of the guinea pig. Acta Otolaryngol (Stockh) [Suppl] 95 : 149-158
5. Guild SR (1927) The circulation of the endolymph. Am J Anat 39 : 57-81 6. Hallpike C, Cairns H (1938) Observations on the pathology of Meniere's syndrome. J Laryngol Otol 53 : 625-655 7. Ishii T, Silverstein H, Balogh K Jr (1966) Metabolic activities of the endolymphatic sac. Acta Otolaryngol (Stockh) 62:6173 8. Kimura RS, Schuknecht HF (1965) Membranous hydrops in the inner ear of the guinea pig after obliteration of the endolymphatic sac. Pract Otorhinolaryngol 27 : 343-354 9. Kimura RS, Schuknecht HF, Ota CY, Jones DD (1980) Obliteration of the ductus reuniens. Acta Otolaryngol (Stockh) 89: 295-309 10. Lundquist P-G (1976) Aspects on endolymphatic sac morphology and function. Arch Otorhinolaryngol 212 : 231-240 11. Portmann G (1927) Vertigo. Surgical treatment by opening of the saccus endolymphaticus. Arch Otolaryngol 6:309-315 12. Schuknecht HF (1977) Pathology of Meniere's disease as it relates to the sac and tack procedures. Ann Otol Rhinol Laryngol 86: 677-682 13. Schuknecht HF (1989) Meniere's disease. In: English JM (ed) Otolaryngology. Lippincott, Philadelphia, pp 1-23 14. Schuknecht HF, Seifi AE (1963) Experimental observations on the fluid physiology of the inner ear. Ann Otol Rhinol Laryngol 72 : 687-712 15. Schuknecht HF, Northrop C, Igarashi M (1968) Cochlear pathology after destruction of the endolymphatic sac in the cat. Acta Otolaryngol (Stockh) 65 : 479-487 16. Silverstein H (1966) Biochemical and physiologic studies of the endolymphatic sac in the cat. Laryngoscope 76:498-512 17. Thomsen J, Bretlau P (1986) General conclusions. In: Pfaltz CR (ed) Controversial aspects of Meniere's disease. Thieme, New York, pp 120-136 18. Torok N (1977) Old and new in Meniere's disease. Laryngoscope 87 : 1870-1877 19. Wladislavosky-WasermanP, Facer GW, Mokri B, Kurland LT (1984) Meniere's disease: a 30-year epidemiologic and clinical study in Rochester, MN, 1951-1980. Laryngoscope 94:10981102 20. Yamakawa K (1938) The inner ear of a patient with Meniere's syndrome. J Otorhinolaryngol Soc Jpn 44:2310-2312
