Abstract
Purpose
The aim of the study is to probe whether intratympanically gadolinium contrast-enhanced three-dimensional fluid-attenuated inversion recovery magnetic resonance imaging, together with magnetic resonance imaging scoring system of the perilymphatic space, had advantages in diagnosing patients with bilateral Meniere’s disease.
Materials and methods
Eight patients diagnosed as ‘definite’ bilateral Meniere’s disease and two patients considered as ‘possible’ Meniere’s disease were selected for the current study. All ten patients underwent caloric test, vestibular evoked myogenic potential and intratympanically gadolinium-enhanced magnetic resonance imaging. The perilymphatic space of scanned images were analyzed to investigate the presence of endolymphatic hydrops. The positive rates (bilaterally abnormal patients/patients tested) of the three examinations in the eight patients with bilateral Meniere’s disease were calculated respectively. We also selected eight patients with unilateral Meniere’s disease as the control group by the method of simple random sampling without replacement.
Results
According to the magnetic resonance imaging scoring system, 100% (8/8) of the patients with bilateral Meniere’s disease had bilateral endolymphatic hydrops. The positive rates of vestibular evoked myogenic potential and caloric test were 50% (4/8) and 25% (2/8), respectively. There was a significant difference among the positive rates of the three examinations ( P < .05). Two patients with ‘possible’ Meniere’s disease had bilateral endolymphatic hydrops by magnetic resonance imaging. Eight patients with unilateral Meniere’s disease displayed endolymphatic hydrops of the affected ears.
Conclusions
Intratympanically gadolinium-enhanced magnetic resonance imaging has a relatively high positive rate of exhibiting bilateral endolymphatic hydrops. This technique with the magnetic resonance imaging scoring system is valuable when diagnosing bilateral Meniere’s disease.
1
Introduction
Meniere’s disease (MD) is clinically characterized by recurrent spontaneous attacks of vertigo, fluctuating hearing loss, tinnitus, and aural fullness. This syndrome was firstly described by Prosper Meniere in 1861, which he attributed to a labyrinthine disorder. The histopathological change of MD is endolymphatic hydrops.
Diagnosis of MD is essentially clinical in nature. In 1995, the hearing and balance committee of the American Academy of Otolaryngology and Head and Neck Surgery (AAO-HNS) enhanced the diagnostic criteria, making them simple and more easily applicable . According to AAO-HNS criteria, individuals with 2 or more spontaneous vertigo spells, lasting for 20 minutes or more, with documented hearing loss in at least one occasion and tinnitus or ear fullness are clinically classified as having Meniere’s disease . Diagnosis certainty is only possible by means of a post mortem study of the temporal bone . It was found that patients with bilateral MD had symptoms earlier than patients with unilateral disease and there was no difference between the two groups in duration of disease and associated symptoms . It is a consensus among many authors that, the longer the disease progression time, the greater is the percentage of bilateral involvement . When in the cases of bilateral sensorineural deafness with episodes of MD-like vertigo, making a diagnosis of bilateral MD is sometimes difficult if the diagnostic tests only provide clues about the abnormality of one side.
At present, the technique of diagnosing MD is mainly composed of audiological and vestibular function examinations. Various methods of examination, such as the glycerol test, electrocochleogram (ECoG), caloric test and vestibular evoked myogenic potential (VEMP), provide sufficient experimental data for diagnosing endolymphatic hydrops. In the area of imaging technology, routine high-resolution magnetic resonance imaging (MRI) hydrography of the inner ear alone cannot identify endolymphatic hydrops in MD patients. In 2007, Nakashima and colleagues successfully used three-dimensional (3D) fluid-attenuated inversion recovery (FLAIR) MRI after intratympanic gadolinium injection to image the perilymphatic space of the inner ear for identifying whether there was endolymphatic hydrops . In 2012, Fang et al. proposed two simple and effective MRI scoring methods for diagnosing endolymphatic hydrops.
Whether intratympanically gadolinium-enhanced MRI has an advantage over other diagnostic tests for bilateral MD (e.g. caloric test and VEMP) is worth investigating. In the current study, we applied intratympanic injection of gadolinium–diethylenetriamine penta-acetic acid (Gd-DTPA)–dimeglumine solution in 8 patients clinically diagnosed as ‘definite’ bilateral MD and 2 patients considered as ‘possible’ MD and performed inner-ear 3D-FLAIR MRI scanning. In comparison with the results of caloric test and VEMP, we want to probe the value of this MRI technique in diagnosing bilateral MD.
2
Materials and methods
2.1
Clinical data
One hundred twenty-three patients were clinically diagnosed as ‘definite’ MD in the Department of Otolaryngology–Head and Neck Surgery of the First Affiliated Hospital of Fujian Medical University from January 2010 to September 2013 and 8 patients with ‘definite’ bilateral MD among them were selected for the current study. Meanwhile, we selected 8 patients from the 115 unilateral MD patients as the control group by the method of simple random sampling without replacement. The diagnostic criteria of unilateral or bilateral MD are based on the AAO-HNS guidelines . During the same period, two patients with episodes of MD-like vertigo were regarded as ‘possible’ MD because they did not have documented hearing loss of unilateral or bilateral ears in at least one occasion.
There were 6 males and 2 females among the bilateral MD patients, with a mean visiting age of 43.63 ± 13.03 years (range of 29 to 60 years). In all 18 patients, intratympanic injection of Gd-DTPA-dimeglumine solution was carried out within 1 week after the last episode of vertigo. The ear canal and eardrum were intact before injection. Eight patients with ‘definite’ bilateral MD and two patients with ‘possible’ MD also underwent caloric test and VEMP testing. This study was approved by the internal review board of our hospital, and all participating patients gave written informed consent to their participation in the study, which followed the ethical guidelines of the Declaration of Helsinki.
2.2
Methods
2.2.1
MRI examination
Gd-DTPA-dimeglumine solution (Magnevist; Schering AG, Guangzhou, China) was used as the contrast medium. Gadolinium hydrate diluted eightfold with saline was injected through the tympanic membrane (using a 23-gauge needle) in 36 ears of 18 patients. The patient was kept with the head rotated 45° contralaterally for 30 minutes after the injection. Twenty-four hours later, 3D-FLAIR MRI, using a 3.0-Tesla unit, was performed by a radiologist according to a protocol. MRI was performed with a Verio 3.0-Tesla 16-channel head system (Siemens, Erlangen, Germany).
The following images were obtained:
Routine sagittal Turbo SE T2-weighted images were taken via the internal auditory canal. This view not only helped exclude intracranial and cerebellopontine angle lesions, but also aided positioning for further high-resolution labyrinth scans.
Routine MRI hydrography of the inner ear [three-dimensional Sampling Perfection with Application-optimized Contrast using different flip angle Evolutions (3D-SPACE)] was performed, and served as a reference for labyrinth anatomy.
Isotropic 3D-SPACE-FLAIR was also performed.
2.2.2
Image postprocessing and evaluation of endolymphatic hydrops
Routine hydrography images were processed with three-dimensional, multiplanar reconstruction and maximum intensity projection, using the Syngo suite (Siemens, Erlangen, Germany). Using labyrinth hydrography as the anatomical reference, gadolinium distribution in the labyrinth was quantitatively scored by two professional radiologists in an independent, double-blinded manner. The scoring results were compared to reduce bias and the final decisions were made by consensus. The scoring criteria are shown in Table 1 . A score of three in the vestibular reflected a low-signal saccule image found medial to the vestibule below the horizontal semicircular canal, accompanied by a normal image of the vestibule above the horizontal semicircular canal, together with a dumbbell-shaped utricle.
| Appearance | Cochlea | Vestibule | Semicircular canals | ||||
|---|---|---|---|---|---|---|---|
| Base | Middle | Apex | Superior | Horizontal | Posterior | ||
| Not visible a | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Partially visible b | 1 | 1 | 1 | 3 | 1 | 1 | 1 |
| Completely visible c | 2 | 2 | 2 | 6 | 2 | 2 | 2 |
a Absence of high-signal contrast medium.
b Failure to show high-signal image of entire cochlear canal, or high-signal image of cochlear canal limited to tympanic or vestibular scale, or interrupted high-signal images of semicircular canals, or incomplete high-signal image of vestibule.
Based on the MRI scoring system which was proposed for the diagnosis of endolymphatic hydrops by Fang et al. , the presence of endolymphatic hydrops on the imaging aspects was evaluated in these bilateral MD patients. One scoring method was based on the scores of the different labyrinth components, as follows: if the result of the function (65.026 − 0.418 × cochlear score − 7.938 × vestibular score − 3.939 × semicircular canal score) reaches 0.3982299, a diagnosis of endolymphatic hydrops can be made. Based on the above formula, a vestibular score of three or lower would cause the final result to rise higher than the cut-off point, regardless of the semicircular canal or cochlear score; therefore, endolymphatic hydrops could be diagnosed directly in this situation. The other diagnostic method was based on the total MRI scores. When the direct sum of all scores from different aspects fell below 14.5, a diagnosis of endolymphatic hydrops could be established.
2.2.3
Pure tone audiometry and electrocochleogram
An OB922 pure tone audiometer (Madsen, Copenhagen, Denmark) was used. The measurement was carried out by the ‘up-and-down’ method (i.e. up 5 dB, down 5 dB). According to the American diagnostic criteria in 1995, in the bilaterally affected cases, if each ear had the pure-tone threshold average of 4 frequencies of 0.5, 1.0, 2.0 and 3.0 kHz greater than 25 dB, we could consider the result of pure tone audiometry as abnormal.
ECoG was conducted using a VikingQuest evoked potential system (Nicolet, Madison, Wisconsin, USA). The stimulating electrodes were placed outside the tympanum and –summating potential/action potential (− SP/AP) > 0.40 was considered to be abnormal.
2.2.4
Procedures and diagnostic standards of caloric test and VEMP testing
2.2.4.1
Caloric test
The patient was placed in a 30° head-up supine position. The ear was examined by infusing 25 °C cold air and 46 °C hot air using a Varioair caloric stimulator (Atmos, Lenzkirch, Germany). Nystagmus was recorded after the infusion using infrared video cameras (Ulmer video-nystagmography (VNG) system; Synapsys, Marseilles, France). A canal paresis (CP) value more than 25% was considered to be abnormal.
2.2.4.2
VEMP testing
The patient was placed in the supine position and asked to raise his or her head during measurement to maintain tonic contraction of the sternocleidomastoid muscle. VEMP was recorded under bilateral click stimulation. The stimulating sound was a 0.1 ms click noise, with an intensity of 95 dBnHL, at a rate of 5.1 per second. The bandpass filter frequency ranged from 0.01 to 20.00 kHz, and the stimulating frequency was 100 Hz. The recorded electromyography (EMG) signal was rectified and the difference waveform (reflecting the difference between the EMG recordings of sternocleidomastoid muscle activity with and without click stimulation) was used for analysis. The results were considered abnormal if: the p13–n23 component disappeared, the latency was extended (if the upper limit of p13 latency was ≥ 17.30 ms and/or the upper limit of n23 latency was ≥ 24.62 ms), the ratio of bilateral amplitudes was ≥ 1.61 or the asymmetry amplitude was ≥ 0.29 .
2.2.5
Statistical analysis
The positive rates (bilaterally abnormal patients/patients tested) among intratympanically Gd-enhanced MRI, caloric test and VEMP testing were compared with Cochran Q test, using the SPSS 17.0 software (Chicago, Illinois, USA). A P value of < 0.05 was considered to be statistically significant.
2
Materials and methods
2.1
Clinical data
One hundred twenty-three patients were clinically diagnosed as ‘definite’ MD in the Department of Otolaryngology–Head and Neck Surgery of the First Affiliated Hospital of Fujian Medical University from January 2010 to September 2013 and 8 patients with ‘definite’ bilateral MD among them were selected for the current study. Meanwhile, we selected 8 patients from the 115 unilateral MD patients as the control group by the method of simple random sampling without replacement. The diagnostic criteria of unilateral or bilateral MD are based on the AAO-HNS guidelines . During the same period, two patients with episodes of MD-like vertigo were regarded as ‘possible’ MD because they did not have documented hearing loss of unilateral or bilateral ears in at least one occasion.
There were 6 males and 2 females among the bilateral MD patients, with a mean visiting age of 43.63 ± 13.03 years (range of 29 to 60 years). In all 18 patients, intratympanic injection of Gd-DTPA-dimeglumine solution was carried out within 1 week after the last episode of vertigo. The ear canal and eardrum were intact before injection. Eight patients with ‘definite’ bilateral MD and two patients with ‘possible’ MD also underwent caloric test and VEMP testing. This study was approved by the internal review board of our hospital, and all participating patients gave written informed consent to their participation in the study, which followed the ethical guidelines of the Declaration of Helsinki.
2.2
Methods
2.2.1
MRI examination
Gd-DTPA-dimeglumine solution (Magnevist; Schering AG, Guangzhou, China) was used as the contrast medium. Gadolinium hydrate diluted eightfold with saline was injected through the tympanic membrane (using a 23-gauge needle) in 36 ears of 18 patients. The patient was kept with the head rotated 45° contralaterally for 30 minutes after the injection. Twenty-four hours later, 3D-FLAIR MRI, using a 3.0-Tesla unit, was performed by a radiologist according to a protocol. MRI was performed with a Verio 3.0-Tesla 16-channel head system (Siemens, Erlangen, Germany).
The following images were obtained:
Routine sagittal Turbo SE T2-weighted images were taken via the internal auditory canal. This view not only helped exclude intracranial and cerebellopontine angle lesions, but also aided positioning for further high-resolution labyrinth scans.
Routine MRI hydrography of the inner ear [three-dimensional Sampling Perfection with Application-optimized Contrast using different flip angle Evolutions (3D-SPACE)] was performed, and served as a reference for labyrinth anatomy.
Isotropic 3D-SPACE-FLAIR was also performed.
2.2.2
Image postprocessing and evaluation of endolymphatic hydrops
Routine hydrography images were processed with three-dimensional, multiplanar reconstruction and maximum intensity projection, using the Syngo suite (Siemens, Erlangen, Germany). Using labyrinth hydrography as the anatomical reference, gadolinium distribution in the labyrinth was quantitatively scored by two professional radiologists in an independent, double-blinded manner. The scoring results were compared to reduce bias and the final decisions were made by consensus. The scoring criteria are shown in Table 1 . A score of three in the vestibular reflected a low-signal saccule image found medial to the vestibule below the horizontal semicircular canal, accompanied by a normal image of the vestibule above the horizontal semicircular canal, together with a dumbbell-shaped utricle.
| Appearance | Cochlea | Vestibule | Semicircular canals | ||||
|---|---|---|---|---|---|---|---|
| Base | Middle | Apex | Superior | Horizontal | Posterior | ||
| Not visible a | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Partially visible b | 1 | 1 | 1 | 3 | 1 | 1 | 1 |
| Completely visible c | 2 | 2 | 2 | 6 | 2 | 2 | 2 |
a Absence of high-signal contrast medium.
b Failure to show high-signal image of entire cochlear canal, or high-signal image of cochlear canal limited to tympanic or vestibular scale, or interrupted high-signal images of semicircular canals, or incomplete high-signal image of vestibule.
Based on the MRI scoring system which was proposed for the diagnosis of endolymphatic hydrops by Fang et al. , the presence of endolymphatic hydrops on the imaging aspects was evaluated in these bilateral MD patients. One scoring method was based on the scores of the different labyrinth components, as follows: if the result of the function (65.026 − 0.418 × cochlear score − 7.938 × vestibular score − 3.939 × semicircular canal score) reaches 0.3982299, a diagnosis of endolymphatic hydrops can be made. Based on the above formula, a vestibular score of three or lower would cause the final result to rise higher than the cut-off point, regardless of the semicircular canal or cochlear score; therefore, endolymphatic hydrops could be diagnosed directly in this situation. The other diagnostic method was based on the total MRI scores. When the direct sum of all scores from different aspects fell below 14.5, a diagnosis of endolymphatic hydrops could be established.
2.2.3
Pure tone audiometry and electrocochleogram
An OB922 pure tone audiometer (Madsen, Copenhagen, Denmark) was used. The measurement was carried out by the ‘up-and-down’ method (i.e. up 5 dB, down 5 dB). According to the American diagnostic criteria in 1995, in the bilaterally affected cases, if each ear had the pure-tone threshold average of 4 frequencies of 0.5, 1.0, 2.0 and 3.0 kHz greater than 25 dB, we could consider the result of pure tone audiometry as abnormal.
ECoG was conducted using a VikingQuest evoked potential system (Nicolet, Madison, Wisconsin, USA). The stimulating electrodes were placed outside the tympanum and –summating potential/action potential (− SP/AP) > 0.40 was considered to be abnormal.
2.2.4
Procedures and diagnostic standards of caloric test and VEMP testing
2.2.4.1
Caloric test
The patient was placed in a 30° head-up supine position. The ear was examined by infusing 25 °C cold air and 46 °C hot air using a Varioair caloric stimulator (Atmos, Lenzkirch, Germany). Nystagmus was recorded after the infusion using infrared video cameras (Ulmer video-nystagmography (VNG) system; Synapsys, Marseilles, France). A canal paresis (CP) value more than 25% was considered to be abnormal.
2.2.4.2
VEMP testing
The patient was placed in the supine position and asked to raise his or her head during measurement to maintain tonic contraction of the sternocleidomastoid muscle. VEMP was recorded under bilateral click stimulation. The stimulating sound was a 0.1 ms click noise, with an intensity of 95 dBnHL, at a rate of 5.1 per second. The bandpass filter frequency ranged from 0.01 to 20.00 kHz, and the stimulating frequency was 100 Hz. The recorded electromyography (EMG) signal was rectified and the difference waveform (reflecting the difference between the EMG recordings of sternocleidomastoid muscle activity with and without click stimulation) was used for analysis. The results were considered abnormal if: the p13–n23 component disappeared, the latency was extended (if the upper limit of p13 latency was ≥ 17.30 ms and/or the upper limit of n23 latency was ≥ 24.62 ms), the ratio of bilateral amplitudes was ≥ 1.61 or the asymmetry amplitude was ≥ 0.29 .
2.2.5
Statistical analysis
The positive rates (bilaterally abnormal patients/patients tested) among intratympanically Gd-enhanced MRI, caloric test and VEMP testing were compared with Cochran Q test, using the SPSS 17.0 software (Chicago, Illinois, USA). A P value of < 0.05 was considered to be statistically significant.
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