Introduction
Inner-ear anomalies are frequently found in patients with sensorineural hearing loss. In cases of posterior inner-ear malformation, aplasia and/or dysplasia of the lateral semicircular canal (LSC) are the most commonly encountered anomalies of the vestibular apparatus, second only to large vestibular aqueduct malformation.Reference Johnson and Lawlani1 Their impact on balance, however, especially in cases with no hearing loss, is to date far from clear. For this reason, the real role of these kinds of malformation in cases of imbalance or even of vertigo is unpredictable. Most of the relevant medical literature contains only data regarding the impact of inner-ear malformation on hearing status. In this regard, radiographic studies of the temporal bone may show osseous anatomical abnormalities in up to 30 per cent of patients with congenital sensorineural hearing loss (SNHL).Reference Antonelli, Varela and Mancuso2 However, most inner-ear malformations accounting for SNHL are purely membranous, and, for this reason, it has been stated that they can be detected only in histological sections.Reference Yu, Mukherji, Carrasco, Pillsbury and Shores3, Reference Rodriguez, Shah and Kenna4 We partially disagree with this view, since we believe that high-resolution magnetic resonance imaging (MRI) is capable of visualising the entire architecture of the inner ear and can certainly detect inner-ear anomalies. Our previous findings confirmed this opinion.Reference Dallan, Bruschini, Neri, Nacci, Segnini and Rognini5–Reference Neri, Berrettini, Panconi, Caramella and Bartolozzi7
From an embryological point of view, it seems reasonable to classify inner-ear anomalies according to their likely development during embryogenesis. Based on the monumental work of Jackler et al.,Reference Jackler, Luxford and House8 it has become accepted that malformations arise as a result of arrested development at a specific point in embryogenesis; for this reason, malformations have been classified according to the stage of hypothetical embryological arrest. Usually, vestibular malformations are associated with large vestibular aqueduct and cochlear malformations, due to the fact that their development occurs during the same weeks of gestation. On the other hand, it has been reported that isolated arrest of the development of the cochlea or the semicircular canals can occur.Reference Parnes and Chernoff9 This seems possible, given the fact that development of these structures is dependent on many genes, several of which are specific for either one or the other.
We report our experience with a patient with vestibular complaints, normal hearing and LSC malformation. A review of the literature and speculative considerations are also given.
Case report
A 38-year-old Caucasian man with a few months' history of recurrent sensations of imbalance, but without typical vertigo, was admitted to our department. Postural instability with linear tilting was experienced. The patient's history was negative for systemic diseases, recent head trauma and drug consumption. A familial history of migraine was reported.
Bedside vestibular examination revealed nothing more than a mild, left-directed, head-shaking nystagmus with a mild vertical component. The bithermal caloric test demonstrated a unilateral, right vestibular paresis. Vestibular evoked myogenic potential examination was normal, as was pure tone audiometry. Subjective visual vertical evaluation with stationary testing demonstrated an impaired utricular function with the right side more involved. Tests for visual-ocular control (smooth pursuit and saccadic eye movements) were within normal limits. No mutation in connexin 26 and 30 genes was found on genetic evaluation. Neuroimages were performed. No central nervous system pathology or tumour involving the vestibular area was observed. High-resolution MRI evaluation of the inner ear, with native images and three-dimensional reconstruction, demonstrated severe ectasia of the utricle on the right side, with near-total aplasia of the lateral semicircular canal (LSC) (Figure 1a). On the left side, mild ectasia of the utricle and the LSC was seen (Figure 1b).
Fig. 1 Magnetic resonance imaging reconstructions of the inner ear. (a) Right side, showing severe ectasia of the utricle with near-total aplasia of the lateral semicircular canal. (b) Left side, showing mild ectasia of the utricle and lateral semicircular canal.
Overall, the left side anomalies were much less severe than those on the right. A short course of vestibular rehabilitation was performed, resulting in clear improvement of the presenting symptoms. Computed tomography scanning showed bony inner-ear anomalies compatible with those described above (Figure 2).
Fig. 2 Axial computed tomography scan showing bony anomalies of both inner ears. On the right side, severe ectasia of the vestibule is seen, with no visible lateral semicircular canal. On the left side, mild ectasia of the vestibule and the lateral semicircular canal is evident.
Discussion
Inner-ear malformations which impact on hearing status have been extensively studied. However, little research has been performed on limited vestibular anomalies in patients without hearing impairment. Since the first report by Parnes and Chernoff,Reference Parnes and Chernoff9 it has seemed clear that selective vestibular malformation can coexist with a normal or near-normal cochlea. However, existing data indicate that patients with lateral semicircular canal (LSC) malformation may present with sensorineural, mixed and conductive hearing loss.Reference Rodriguez, Shah and Kenna4 In the largest series published to date, none of the patients with LSC anomalies had normal hearing. In that series, no pure tone audiometry result better than 55 dB was obtained at the time of the initial examination. It has been stated that the hearing loss associated with semicircular canal anomalies is probably due to anomalous membranous labyrinth development.Reference Yu, Mukherji, Carrasco, Pillsbury and Shores3
To the best of our knowledge, selective LSC malformation with normal hearing has not previously been reported. Our case, in which a selective bony-membranous vestibular anomaly was present with no hearing impairment, seems to demonstrate an independent development of the individual semicircular canal in relation to the other inner structures. Hence, this appears to indicate a more complex embryological process than merely arrested development, as previously thought.
On these grounds, it can be assumed that a myriad of inner-ear malformations may result from aberrant rather than arrested development. A detailed description of inner-ear embryogenesis is beyond the scope of this paper, and has been previously and excellently performed by Kenna and Hirose.Reference Kenna, Hirose, Bluestone, Stool and Alpert10 As is well known, in the past it was accepted that malformations arose as a result of arrested development at a specific stage of embryogenesis.Reference Jackler, Luxford and House8 However, many findings challenge this statement. Although it is possible that the LSC is more often involved, given its later embryonic development with respect to the superior and posterior semicircular canals, the possibility of fine, accurate control of inner-ear subunit development at a molecular level seems more reasonable. Furthermore, it has been proposed that the cochlea and the vestibules develop via independent mechanisms and do not interchange critical information during their developmental course. Many data on animal genetic patterns are now available on this topic. Mutations in otx1 lead to isolated malformations of the LSC and lateral ampulla,Reference Morsli, Tuorto, Choo, Postiglione, Simeone and Wu11 and it has been reported that Nkx5-1 mutations preferentially affect the LSC.Reference Hadrys, Braun, Rinkwitz-Brandt, Arnold and Bober12 In this respect, Nkx5-1 mutant mice show no defects in hearing ability nor present any morphological or histological abnormalities of the cochlea. It has been stated that Nkx5-1, otx1 and prx1/prx2 are responsible for LSC formation, and their human homologues may be mutated in patients with LSC malformations.
Our case raises the question of how frequently selective vestibular anomalies appear in people with normal hearing and vestibular complaints. Obviously, our report cannot answer this question. However, since many patients with SNHL are found to have cochlear anomalies when correctly investigated, it seems reasonable to consider that, at least in a minimal percentage, patients with disequilibrium and/or vertigo might have limited vestibular malformations without hearing impairment. We believe that, although speculative, this hypothesis is worthy of consideration. Our patient seems to confirm this possibility; he complained of no hearing deficit, only of unbalance and dizziness. Neuro-otological investigations, with bithermal caloric testing, vestibular evoked myogenic potentials and subjective visual vertical testing, demonstrated peripheral involvement of the vestibular system, with functional impairment of the LSC and utricle. Native images and three-dimensional reconstruction of the inner ear showed vestibular malformations limited to the utricle and LSC (Figure 1).
• Inner-ear malformations are frequently found in patients with sensorineural hearing loss
• Lateral semicircular canal malformations are usually associated with other inner-ear malformations and described in patients with hearing loss
• Lateral semicircular canal malformation can be associated with peripheral involvement of the vestibular system, regardless of hearing status
• Isolated vestibular malformation might not be as rare as previously thought among patients with recurrent peripheral vertigo, and should be investigated with the aid of sophisticated imaging techniques
The dearth of medical literature regarding this topic may be due to the limits encountered in visualisation of the inner ear. During the 1980s and 1990s, direct visualisation of bony inner-ear structures was very difficult, and that of the membranous inner ear was almost impossible. In this respect, the real limit of radiological evaluation in the past was related exclusively to bone evaluation, due to technical inadequacy – all membranous anomalies remained hidden and undetectable. Although many authors have stated, even recently, that membranous malformations can only be seen in histological sections,Reference Yu, Mukherji, Carrasco, Pillsbury and Shores3, Reference Rodriguez, Shah and Kenna4 we believe that complete three-dimensional reconstruction of the inner-ear architecture is not only feasible but in fact allows good visualisation of the different subunits. Based on our experience, although almost all anecdotal, we confirm (in agreement with others)Reference Neri, Caramella, Cosottini, Zampa, Jackson and Berrettini6, Reference Neri, Berrettini, Panconi, Caramella and Bartolozzi7 the utility and efficacy of high-resolution MRI with three-dimensional reconstruction for visualising inner-ear morphology.
Also in agreement with others,Reference Yu, Mukherji, Carrasco, Pillsbury and Shores3 we believe that anomalies of inner-ear morphology are probably not simply a result of embryogenesis arrest. Further studies, at a molecular level and with the aid of sophisticated neuroimaging techniques, will greatly aid the understanding of this fascinating and obscure field.
Conclusion
Inner-ear malformations account for many cases of sensorineural hearing impairment. Scanty data are available regarding the impact of vestibular malformation on vestibular symptoms. High-resolution MRI is very useful for visualising inner-ear morphology, and for this reason can help in detecting vestibular anomalies. Based on the complexity of inner-ear development, it is reasonable to believe that anomalies in inner-ear development are probably not simply the result of arrested embryogenesis. Further studies with molecular analysis and high-resolution, three-dimensional reconstruction are needed in order to better understand the field of inner-ear malformations and development.
