Keywords
Ménière disease - temporal bone - x-ray computed tomography
Introduction
Ménière disease (MD) is a chronic disease affecting the inner ear. It was first described,
in 1861, by Prosper Ménière, and it is broadly characterized by intermittent episodes
of vertigo, fluctuating hearing loss, tinnitus and aural fullness.[1]
[2]
Data concerning the incidence and prevalence of MD are scarce and uncertain.[3] Prevalence estimates ranges from 10 to 150 per 100,000 individuals.[4] Most of the studies suggest a slight preponderance of the disease among women (1.3
women per each affected man).[5] Ménière disease also seems more frequent among adults in their fourth or fifth decades
of life and positive family history is extremely common.[6]
[7]
The diagnosis of Ménière disease remains eminently clinical.[8] Its clinical presentation is widely variable. Many patients present with audiological
symptoms, some have mostly vestibular complaints and others show a combination of
audiovestibular manifestations.[9] Bilateral involvement might be seen in 10–50% of the patients, leading to a difficult-to-treat
condition with more disabling symptoms and unfavorable prognosis.[10] In 2015, the Classification Committee of the Bárány Society, the Japan Society for
Equilibrium Research, the European Academy of Otology and Neurotology (EAONO), the
Equilibrium Committee of the American Academy of Otolaryngology-Head and Neck Surgery
(AAO-HNS) and the Korean Balance Society jointly revised the diagnostic criteria and
established a new classification for MD.([Table 1])[11] These criteria remain as the main diagnostic tool for MD in clinical practice.
Table 1
Diagnosis criteria and classification of Ménière disease according to the Classification
Committee of the Bárány Society, the Japan Society for Equilibrium Research, the European
Academy of Otology and Neurotology (EAONO), the Equilibrium Committee of the American
Academy of Otolaryngology-Head and Neck Surgery (AAO-HNS) and the Korean Balance Society[11]
|
DIAGNOSIS CRITERIA FOR MÉNIÈRE DISEASE
|
|
Definite Ménière disease:
• Two or more spontaneous vertigo episodes, each of them lasting from 20 minutes
to 12 hours.
• Audiometrically documented low- to medium- frequency sensorineural hearing loss
in one ear, defining the affected ear on at least one occasion before, during or after
one of the episodes of vertigo.
• Fluctuating aural symptoms (hearing loss, tinnitus, aural fullness) in the affected
ear
• Not better accounted for by another vestibular diagnosis
|
|
Probable Ménière disease:
• Two or more spontaneous vertigo episodes, each of them lasting from 20 minutes
to 12 hours.
• Fluctuating aural symptoms (hearing loss, tinnitus, aural fullness) in the affected
ear
• Not better accounted for by another vestibular diagnosis
|
However, some authors report that evidences of endolymphatic hydrops, obtained in
particular complementary investigation methods with growing sensibility and specificity,
might be helpful in patients with MD in its early stage or those with mild and non-specific
symptoms.
The possibility of clinical implications of the anatomical variations of the temporal
bone among patients with MD has been targeted in some studies. Recent technological
advances, unique special resolution and wide availability have made high resolution
computed tomography (HRCT) of the temporal bone the main imaging modality in otology.[12] High resolution computed tomography is capable of detecting anatomical correlations
between the structures of the inner ear, including surrounding vascular components.
As a result, it can define, with high sensibility and specificity rates, anatomical
variations which, among patients with MD, might serve as clinical markers that could
underpin the diagnosis of this condition or play a role in its pathophysiology.
No radiological sign is deemed specific for MD. Previous studies have shown higher
prevalence of some anatomical variations in the temporal bones of affected individuals,
although they vary significantly in terms of the variables evaluated, the radiological
method employed and the stratification of the sample. Yet, there are few researches
including patients with bilateral MD.
This present study aims to identify anatomical variations of the temporal bone which
might be associated with unilateral and/or bilateral MD.
Methods
This is a case-control study. All included participants (n = 37) attended ambulatories of otoneurology in a public tertiary hospital and a specialized
clinic in Curitiba, Brazil, and underwent a computed tomography (CT) of the temporal
bone as a complementary evaluation. For the study, each ear was considered separately
(n
final= 74). Hence, a case group (group A, n
A = 33) consisted of the affected ears of patients with clinical diagnosis of unilateral
or bilateral MD, according to the new criteria proposed by international societies
in 2015, which includes, by definition, suggestive and audiometrically documented
hearing loss. A control group (group B, n
B = 41) included the ears of individuals attending the same clinics, although without
criteria for either probable or definite MD and presenting a normal audiometry, as
well as the contralateral ears of the patients with unilateral MD included in the
case group. Patients under 18 years of age or with history of inflammatory otitis
media, temporal bone neoplasm or trauma, congenital ear anomalies or previous otologic
surgery were excluded from the sample. All included participants signed a free and
informed consent form. The project was approved and registered by the Institutional
Ethics Committee (CAAE number, 54235316.9.0000.0096).
The tomographic images were obtained in a matrix of 512 × 512 pixels, in high resolution,
between 2014 and 2016. The HRCT scans provided volumetric images in the axial plane,
which were transferred to a workstation for post-processing. These data were reformatted
in the axial and coronal planes using specific software, yielding images with 1 mm
section thickness on each side individually.
Clinical and epidemiological data were collected from the participants and their images
were assessed by a single radiologist specialized in temporal bone evaluation, without
previous knowledge of their clinical history or physical examination. Anatomical aspects
regarding region-specific temporal bone pneumatization, the jugular bulb and the positioning
and structure of the cochlear and vestibular aqueducts were systematically analyzed.
([Table 2], [Fig. 1])
Fig. 1 Computed axial tomography images showing anatomical variations of the temporal bone:
(A) High jugular bulb, above the level of the tympanic annulus (arrow); (B) Jugular
bulb diverticulum (arrow); (C) Contact between the jugular bulb and the vestibular
aqueduct (arrow); (D) Asymmetric pneumatization of the retrolabyrinthine space, deemed
increased on the right (D1) and decreased on the left side (D2) (arrow). Source: the
author.
Table 2
Variables individually investigated in each ear of this study's sample
|
Anatomical Aspect
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Categories/Unity of Measurement for the Variable
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Categorical Variables
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Height of the jugular bulb considering the basal turn of the cochlea
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High or normal
|
|
Presence of any of the major anatomical variations of the jugular bulb: diverticulum,
dehiscence to the middle ear or otic capsule, contact with cochlear or vestibular
aqueducts
|
Present or absent
|
|
Position of the aperture opening of the vestibular aqueduct
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Above or below the basal turn of the cochlea
|
|
Individualization of the cochlear aqueduct
|
More or less than half of its extension
|
|
Pneumatization of the retrolabyrinthine space
|
Absent/decreased or increased
|
|
Pneumatization of the supralabyrinthine space
|
Absent/decreased or increased
|
|
Pneumatization of the infralabyrinthine space
|
Absent/decreased or increased
|
|
Pneumatization of the petrous apex
|
Absent/decreased or increased
|
|
Continuous Variables
|
|
Anteroposterior diameter of the jugular bulb
|
In millimeters (mm)
|
|
Transverse diameter of the jugular bulb
|
In millimeters (mm)
|
|
Size of the vestibular aqueduct (if visible)
|
In millimeters (mm))
|
|
Inclination angle between the vestibular aqueduct and the vestibule
|
In grades (o)
|
The results from the case and control groups were confronted. A secondary assessment
of the case group was performed after its stratification into two subgroups: one (A1,
n
A1 = 13) composed by the affected ears of patients with unilateral MD and another by
the ears of those with bilateral disease (A2, n
A2 = 20). The control group was also divided into two subgroups, which had their data
compared as well: one (B1, n
B1 = 13) formed by asymptomatic contralateral ears of individuals with unilateral MD
and another (B2, n
B2 = 28) consisting of individuals without MD and normal audiometric evaluation. ([Fig. 2]). Results from subgroups A1 and B1 were also confronted.
Fig. 2 Study flow chart.
The Pearson chi-square and Fisher exact tests were employed to evaluate categorical
variables. Continuous variables were assessed using the Wilcoxon-Mann-Whitney. Statistical
analysis was performed using the Statistical Package for Social Science (SPSS). Significance
level was set at 0.05.
Results
There was no statistical difference between the study groups in terms of age or sex
(p > 0.05, data not shown).
The comparison between the results from the case (A) and control (B) groups is summarized
in [Fig. 3]. There was a significant correlation between MD in only one of the variables assessed:
capacity of individualization of the vestibular aqueduct (VA). Among patients with
MD, this structure was observed less frequently (p = 0.01; Fisher exact test).
Fig. 3 Values (p) for each assessed variable resultant from comparative statistical analysis
between the main study groups, case (A) and control (B). Significance level: p-value < 0.05.
[Table 3] shows the statistical significance level obtained when analyzing subgroups A1 and
A2, which were composed by the affected ears of patients with unilateral and bilateral
MD, respectively. None of the variables was significantly associated with the occurrence
of bilateral disease (p < 0.05).
Table 3
A summary of statistical data (p-value) obtained for each variable after assessing both case subgroups. Comparison
between data of affected ears from patients with unilateral disease (subgroup A1)
and those of individuals with bilateral disease (subgroup A2)
|
Variable
|
p-value
|
|
Presence of high jugular bulb
|
0.41 (χ2)
|
|
Anteroposterior diameter of the jugular bulb
|
0.41 (WCX)
|
|
Transverse diameter of the jugular bulb
|
0.17 (WCX)
|
|
Overall incidence of major variations of the jugular bulb
|
0.63 (Fisher)
|
|
Rate of visualization of the vestibular aqueduct
|
0.13 (Fisher)
|
|
Size of the vestibular aqueduct (if visible)
|
1.0 (WCX)
|
|
Position of the aperture opening of the vestibular aqueduct
|
1.0 (Fisher)
|
|
Inclination angle between the vestibular aqueduct and the vestibule
|
0.57 (WCX)
|
|
Grade of visualization of the cochlear aqueduct
|
1.0 (Fisher)
|
|
Pneumatization of the infralabyrinthine space
|
0.73 (Fisher)
|
|
Pneumatization of the retrolabyrinthine space
|
0.21 (Fisher)
|
|
Pneumatization of the supralabyrinthine space
|
1.0 (Fisher)
|
|
Pneumatization of the petrous apex
|
1.0 (Fisher)
|
Abbreviations: Fisher, Fisher exact test; WCX, Wilcoxon-Mann-Whitney test; χ2: chi-square test.
Significance level: p-value < 0.05.
The results from the statistical analysis between subgroups consisting of the affected
(A1) and healthy contralateral (B1) ears of patients with MD are provided in [Table 4]. Similarly, there was no significant difference for any of the variables investigated.
Table 4
A summary of statistical data (p-value) obtained for each variable when comparing the results of affected ears from
patients with unilateral Ménière disease (subgroup A1) and those of the contralateral
ears of these individuals. (subgroup B1)
|
Variable
|
p-value
|
|
Presence of high jugular bulb
|
1.0 (χ2)
|
|
Anteroposterior diameter of the jugular bulb
|
0.82 (WCX)
|
|
Transverse diameter of the jugular bulb
|
0.45 (WCX)
|
|
Overall incidence of major variations of the jugular bulb
|
0.66 (Fisher)
|
|
Rate of visualization of the vestibular aqueduct
|
1.0 (Fisher)
|
|
Size of the vestibular aqueduct (if visible)
|
0.48 (WCX)
|
|
Position of the aperture opening of the vestibular aqueduct
|
1.0 (Fisher)
|
|
Inclination angle between the vestibular aqueduct and the vestibule
|
0.96 (WCX)
|
|
Grade of visualization of the cochlear aqueduct
|
1.0 (Fisher)
|
|
Pneumatization of the infralabyrinthine space
|
0.69 (Fisher)
|
|
Pneumatization of the retrolabyrinthine space
|
1.0 (Fisher)
|
|
Pneumatization of the supralabyrinthine space
|
1.0 (Fisher)
|
|
Pneumatization of the petrous apex
|
1.0 (Fisher)
|
Abbreviations: Fisher: Fisher exact test; WCX: Wilcoxon-Mann-Whitney test; χ2: chi-square test.
Significance level: p-value < 0.05.
[Fig. 4] reports statistical data regarding the results when comparing the control subgroups
(B1 and B2). There was a trend toward lower angulation between the vestibular aqueduct
and the vestibule in the contralateral ears of patients with unilateral disease, when
compared with the ears of individuals without MD (p = 0.11). Nonetheless, none of the variables reached statistical significance (p < 0.05).
Fig. 4 Results obtained after stratifying the control group: p-value associated with each variable, when comparing the results from the contralateral
ears of patients with unilateral MD (subgroup B1) and those from individuals without
the disease (subgroup B2). Significance level: p-value < 0.05.
Discussion
One previous study has suggested that the sigmoid sinus could be placed significantly
more anteriorly and medially in patients with MD. The authors hypothesized that the
anomalous position of the vessel could generate compression of the endolymphatic sac
and, therefore, hydrops.[13]
The jugular bulb consists of a dilation of the internal jugular vein and is located
at the posterior part of the jugular foramen. When enlarged, it might be responsible
for audiovestibular symptoms.[14] Variations in its size and location are common and might occur due to malformations
in the surrounding bony structure or in the intracranial venous system itself or secondary
to lack of pneumatization of the mastoid portion of the temporal bone. If the jugular
bulb is located superiorly to the inferior surface of the tympanic annulus in the
middle ear, at the level of the basal cochlear turn or less than 2 mm from the inner
auditory channel, it is classified as a high jugular bulb (HJB).[15]
[16] Most of the previous studies that aimed to evaluate HJB have shown limitations,
such as emphasis on its incidence or small samples.[17] Radiological and post-mortem studies of the temporal bone report a prevalence of
HJB ranging from 3–24% of the population, although this variation might not be clinically
apparent.[15]
[17]
[18]
[19] Jugular bulb abnormalities have also been implied in a various range of cochleovestibular
symptoms, depending on the impact on the surrounding structures. The jugular bulb
might erode into the middle ear or into the cochlear or vestibular aqueducts. Hearing
loss, vertigo and tinnitus have also been attributed to high and dehiscent jugular
bulbs, as well as to the compressive effects of HJB on the endolymphatic sac.[18]
[20] A recent German retrospective controlled study has shown a significantly higher
prevalence of jugular bulb abnormalities among patients with MD. The authors concluded
that the temporal bone in these individuals might be constitutionally different and
carry predisposing factors for the development of clinically overt MD.[21] Redfern et al have also described higher prevalence of abnormalities of the jugular
bulb in patients with MD, when compared with the general population.[22] In the present study, differences in the prevalence of HJB or major jugular bulb
abnormalities among affected ears have not been found.
Ikeda e Sando have shown in a study with post-mortem temporal bones that patients
with MD have smaller tube-shaped endolymphatic ducts, in contrast with normal subjects,
whose ducts were bigger and funnel-shaped.[23] Welling et al reported that, in MD, the identification of the endolymphatic duct
on magnetic resonance imaging (MRI) could be significantly less frequent compared
with controls. In this study, the authors also compared the measurements of the temporal
bone in the region of the endolymphatic duct and found smaller dimensions among affected
individuals.[24] By using a systematic approach to the evaluation of CT scans, Alvarenga et al achieved
identification rates of the vestibular aqueduct superior to 90% among both ears of
patients with unilateral MD. The rates did not differ statistically from those of
control individuals.[25] In the present study, among affected ears, there was a significantly greater number
of CT scans in which the vestibular aqueduct could not be individualized (p = 0.01). However, considering only the exams in which this structure was identified,
the absolute measurements did not differ from those of the control arm. No statistically
significant difference between the study groups was obtained regarding either the
position of the internal aperture or the inclination of the vestibular aqueduct. Rates
of identification of the cochlear aqueduct were also similar. As to the assessment
of pneumatization of different portions of the temporal bone, a trend to reduced (p = 0.07, Pearson chi-square test) pneumatization of the retrolabyrinthine space was
observed among subjects with MD, although this result could not be deemed statistically
significant. No difference was demonstrated in the pneumatization of the petrous apex,
infralabyrinthine and supralabyrinthine spaces.
Previous functional studies have shown the presence of abnormal findings in the contralateral
ears of patients with unilateral MD.[26]
[27] These findings have been corroborated by histopathologic studies, which have identified
significantly more damage in the contralateral inner ears of patients with MD compared
with those of normal controls.[28] The incidence of functional contralateral involvement and development of clinically
apparent bilateral MD increases linearly, so that after 30 years of follow-up, up
to 50% of the patients have bilateral disease.[29] Increasing evidence of endolymphatic hydrops in asymptomatic contralateral ears
might suggest that MD is a systemic disease.[30]
[31] Hence, the recurrent findings in the literature of abnormal anatomical features
among both affected and contralateral ears in comparison to normal controls might
indicate that MD has a complex pathophysiology, in which the anatomical component
might be a marker of disease progression or a contributing factor. Accordingly, the
previous existence or the development during follow-up of certain anatomical abnormalities
in the asymptomatic contralateral ear could predispose the patient to the progression
to bilateral disease, with an unfavorable prognosis. Karatas et al studied the size
and width of the endolymphatic duct and the presence of jugular bulb abnormalities
in the CT scans of patients with unilateral MD. In this study, the measurements for
the endolymphatic duct were reported to be smaller and the prevalence of abnormalities
of the jugular bulb was higher among MD patients when compared with healthy controls.
However, for none of the variables, there was a significant difference between the
results of affected and contralateral non-affected ears.[32] Hall et al also described lower periaqueductal pneumatization rates in the CT scans
of patients with MD. Similarly, in this study, the results from the contralateral
ears did not differ from those of the affected ears.[33] Using MRI and CT to evaluate the cochlear aqueduct, Park et al found similar bony
dimensions among the affected ears of patients with MD when compared with a control
group, although fluid length within this structure was significantly decreased among
case subjects. These findings could not be reproduced when comparing the affected
and non-affected ears of patients with MD.[34]
In this work, no statistically significant difference in the prevalence of any anatomical
variations was observed when comparing the affected ears of individuals with unilateral
MD with those of patients with bilateral MD. Thus, the anatomical factor, if important
in MD's pathophysiology and/or diagnosis approach, might contribute independently
of the existence of involvement of both ears. There was no difference when comparing
the results from the affected and the contralateral non-affected ears of patients
with unilateral MD and from these contralateral non-affected ears with the ears of
healthy controls. This finding would indicate that the contralateral ears did not
differ from the affected ears or from the ears of healthy subjects. Longitudinal and
cohort studies might determine more precisely the meaning of these results, as the
possibility of progression of unilateral MD to bilateral disease is well known. Thereby,
it would be necessary to better stratify contralateral ears longitudinally and check
the occurrence of dynamic alterations in the anatomical findings reported according
to the progression of the disease. As a result, it might be possible to establish
the role of the anatomical variations as markers of disease progression or risk factors
for the development of bilateral MD, in case of significant identification of these
variations, late or precociously in the follow-up of contralateral ears that would
become affected over time. Experimental and histopathological studies might define
more clearly the existence of pathophysiological links between anatomical factors
and the incidence of MD, which remain elusive.
Conclusion
Some anatomical variations of the temporal bone might be more frequently found in
routine CT scans from affected ears of patients with MD, such as the lower rates of
individualization of the vestibular aqueduct. Nonetheless, according to the literature,[25] the use of the imaging study of the vestibular aqueduct as a supportive diagnostic
tool and the role of correlated anatomical variations in the development of MD remain
a controversial issue. Longitudinal controlled studies including patients with anatomical
variations possibly related to MD might be important to observe if they develop the
disease more frequently over time.