- Email: [email protected]
Imaging of congenital temporal bone anomalies
Operative Techniques in Otolaryngology (2014) 25, 13–20
Imaging of congenital temporal bone anomalies Ali R. Sepahdari, MD,a Brian D. Zipser, MD,b Michael N. Pakdaman, MDa From the aDepartment of Radiological Sciences, David Geffen SOM, University of California, Los Angeles, California; and the bDepartment of Radiology, Olive View Medical Center, Sylmar, California KEYWORDS Congenital temporal bone anomalies; Pediatric sensorineural hearing loss; Large vestibular aqueduct; CHARGE; Oculoauriculovertebral
A variety of congenital malformations of the ear and temporal bone may be encountered. Anomalies of the inner ear, middle ear, and external auditory canal and auricle can all occur, and there are a variety of clinical presentations that include conductive and sensorineural hearing loss. Some malformations are part of well-described genetic syndromes, whereas others are sporadic. Cochlear implantation may be helpful in some cases. Knowledge of typical patterns of abnormalities can help guide the clinical workup and management plan. The goal of this review is to familiarize the reader with the role of imaging in some of the commonly encountered congenital malformations of the ear and temporal bone. r 2014 Elsevier Inc. All rights reserved.
Introduction When evaluating the pediatric patient with hearing loss, imaging is essential before considering corrective surgery. Congenital anomalies of the temporal bone may produce conductive hearing loss (CHL) or sensorineural hearing loss (SNHL). Imaging is essential in determining whether a patient is likely to benefit from external middle ear corrective surgery in patients with CHL or from cochlear implantation in cases of SNHL and is essential also for guiding workup for a potential underlying genetic syndrome.
Imaging modalities Computed tomography (CT) and magnetic resonance imaging (MRI) are the 2 imaging modalities that are commonly used to evaluate the pediatric patient with hearing loss. Some centers use only 1 modality, whereas others (including our institution) often use both.1 We find CT and MRI to be complementary tests. CT is superior for Address reprint requests and correspondence: Ali R Sepahdari, MD, 757 Westwood Plaza, Suite 1621D, Los Angeles, CA 90095. E-mail address: [email protected]; [email protected] 1043-1810/$ - see front matter r 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.otot.2013.11.003
showing the middle ear anatomy, anomalies of the ossicular chain, and course of the facial nerve canal. Patency of the labyrinthine oval window and round window niche, volume of the middle ear cavity, and anatomical constraints to successful auriculotympano or ossiculoplasty and cochlear implantation are best seen by CT. CT and MRI are similarly sensitive for detecting malformations of the inner ear. Although CT can suggest cochlear nerve deficiency (CND) if the cochlear aperture or internal auditory canal (IAC) is small, MRI is superior in detecting CND through direct visualization of the nerve. Attention to detail is important in ensuring that diagnostic quality images are obtained for both CT and MRI. Close communication between the otologist and the radiologist is helpful in this regard. For CT, it is preferable to perform the studies on a newer model multidetector row scanner (eg, 64 detector row or higher), though high-quality images can still be obtained on older scanners, albeit at the cost of higher radiation dose. It is critical to obtain thinsection images reconstructed in a sharp bone algorithm with a small field of view, ideally with separate small field-ofview reconstructions of the right and left sides separately so as to maximize spatial resolution. With newer model scanners, a volumetric axial acquisition can be reconstructed in the axial and coronal planes and in oblique planes as needed. With older scanners, direct coronal imaging may be
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necessary. When performing MRI, it is of critical importance to obtain high-resolution, 3-dimensional (3D), heavily T2-weighted “cisternographic” sequences to visualize the vestibulocochlear nerves and the labyrinthine structures. These sequences have different names and acronyms according to the MRI manufacturer and the technique that is used to produce the image. Some examples include Constructive Interference in Steady State, Fast Imaging Employing Steady-state Acquisition, 3D DRIVen Equilibrium, T2 Sampling Perfection with Application-optimized Contrasts using different flip angle Evolutions, and Balanced Fast Field Echo. Close communication between the otologist and the radiologist can help ensure that a correct MRI protocol is performed. Sedation is typically required for MRI. CT can often be performed without sedation, particularly with newer scanners that are able to image the entire temporal bone in several seconds.
Syndromic anomalies A variety of genetic syndromes may lead to malformations of the external, middle, and inner ear. Hearing loss may be sensorineural, conductive, or mixed. Certain characteristic patterns of involvement have been described with these conditions, and temporal bone imaging can often guide the genetic workup.
Large vestibular aqueduct syndrome Enlargement of the vestibular aqueduct is the most commonly seen abnormality in pediatric SNHL.2 As this may be a feature of a variety of other syndromic and nonsyndromic malformations, the term large vestibular aqueduct syndrome (LVAS) is typically used to describe
this anomaly when it occurs in isolation or with incomplete cochlear partition (“Mondini” dysplasia) as the only other abnormality. LVAS was first described in 1978 by Valvassori and Clemis3 using polytomography, now an obsolete imaging modality, and later by Hill et al4 using CT. On CT, the characteristic abnormality is enlargement of the vestibular aqueduct (Figure 1). Incomplete cochlear partition (fusion of the middle and apical turns, with missing bony partition [osseous spiral lamina], ie, “Mondini” dysplasia) is a common associated finding, as is mild dysplasia of the lateral semicircular canal (LSC) with associated small LSC bone island.5 On magnetic resonance images, enlargement of both the endolymphatic duct and the endolymphatic sac are evident (Figure 2).6 The typical presentation is of SNHL of varying severity, which may be stable, progressive, or fluctuating.7 Sudden deterioration following trivial head trauma or minor ailments may also be seen.7 Pendred syndrome describes the syndrome of deafness and goiter. Patients with Pendred syndrome typically have abnormal results on perchlorate discharge tests and a mutation of the PDS gene and frequently show radiologic findings of enlarged vestibular aqueduct with incomplete cochlear partition. A recent study showed that many patients with enlarged vestibular aqueducts, but without goiter, have PDS gene mutations,8 suggesting that LVAS and Pendred syndrome lie along a common spectrum. Different criteria have been described for determining whether a vestibular aqueduct is enlarged. Some use an absolute diameter of more than 1.5 mm, measured on axial images at the midpoint between the isthmus and the external aperture, as the cutoff for a normal vestibular aqueduct, basing this on criteria determined from polytomography.3 Some have proposed using cutoffs of more than 0.9 mm at the midpoint or more than 1.9 mm at the external aperture (operculum), termed the “Cincinnati criteria.”2,9 Others
Figure 1 Large vestibular aqueduct syndrome. Axial CT. (A) Image through the level of the lateral semicircular canal shows gross enlargement of the vestibular aqueduct (long arrow). Compare with the posterior semicircular canal (short white arrow) in the same image. (B) Image slightly lower shows cochlear dysplasia with fusion of the middle and apical turns (ie, incomplete partition-II, a.k.a. Mondini dysplasia).
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Figure 2 Large vestibular aqueduct syndrome, same patient as Figure 1. (A) Axial cisternographic T2 MRI shows the same findings. Incomplete cochlear partition (short white arrow) and enlarged vestibular aqueduct (long white arrow) are again noted. Dilation of the endolymphatic sac (long black arrow) is also evident. (B) 3D maximum-intensity projection T2 of the labyrinth shows the dilated endolymphatic sac (ES) and endolymphatic duct (ED).
(including these authors) use the posterior semicircular canal (PSC) as an internal reference marker for size. The PSC, which is well seen at the level of the vestibular aqueduct midpoint, has a diameter of approximately 1.5 cm.10 Using this internal reference marker allows for visual comparison of multiple contiguous images. A measurement of greater than 1 mm at the isthmus of the vestibular aqueduct should also be considered abnormal. Ozgen et al11 noted that measurement of the vestibular aqueduct caliber was more consistent using 451 oblique reconstructions compared with standard axial plane images, though this observation has not resulted in the large-scale revision of criteria for vestibular aqueduct enlargement.
Oculoauricolovertebral spectrum (a.k.a. hemifacial microsomia, craniofacial microsomia, Goldenhar syndrome, and first and second branchial arch anomaly) Oculoauricolovertebral spectrum disorder is a rare, complex, and phenotypically variable birth defect involving the first and second branchial arch derivatives, with estimated prevalence between 1:5,600 and 1:26,650 live births.12 The highly variable phenotype of oculoauricolovertebral spectrum includes craniofacial anomalies and cardiac, vertebral, and central nervous system defects. Most cases are sporadic, but there are rare familial cases that exhibit autosomal dominant inheritance. These patients, unlike those with mandibulofacial dysostosis (Treacher Collins syndrome), typically exhibit an asymmetric deformity of the external ear, small mandible, and hypoplastic or frankly atretic external auditory canal (Figure 3). The severity of the external ear deformity is a basis on which the severity of disease is classified.13 Middle ear anomalies are commonly seen and well characterized.14,15 Inner ear anomalies are less common and include atresia of
the IAC and malformations of the cochlea and semicircular canals.12 CHL is almost always present, with mixed or sensorineural hearing loss being less common.16 Facial nerve palsy may also be seen. In addition to external auditory canal hypoplasia or atresia, which is typically clinically apparent, CT often reveals lateral displacement of the ossicles, malformation of the ossicular chain, low tegmen, and underdevelopment of the mastoid air cells (Figure 3).12,15,17 CT is critical in guiding surgery, as the mastoid segment of the facial nerve canal is typically superficial and more anterior than normal. At times, a congenital cholesteatoma may be present deep to the atretic external auditory canal or at the site of the dysplastic segment of the tympanic part of the temporal bone (Figure 4). CT is critical to detect these lesions, though they may not be detected if the CT is performed too early in life.18
CHARGE syndrome CHARGE syndrome is characterized by a variety of congenital anomalies, including those that compose its name (coloboma, heart anomalies, choanal atresia, mental retardation, genital hypoplasia, and ear anomalies), as well as facial palsy, cleft palate, esophageal atresia, facial dysmorphism, and CNS malformations (Online Mendelian Inheritance in Man, Entry no. 214800). Reports of its prevalence range from 0.2-1.2 every 10,000 live births.19 Major diagnostic criteria are the “4 Cs”: characteristic ear anomaly, coloboma, choanal atresia, and cranial nerve abnormality. The characteristic ear anomaly of CHARGE syndrome is aplasia or hypoplasia of the semicircular canals (Figure 5). Hypoplasia or aplasia of the cochlear nerve is also common in CHARGE syndrome,20 and it is essential to evaluate for this carefully if cochlear implantation is considered (Figures 5 and 6). Other abnormalities include oval or round window atresia or hypoplasia, ossicular dysplasia with ankylosis, cochlear dysplasia, dysplastic or hypoplastic vestibule,
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Figure 3 Oculoauriculovertebral spectrum, that is, Goldenhar syndrome. Coronal CT. (A and B) Normal coronal CT through the right ear. (C) The left external auditory canal is narrowed (arrow) and nearly atretic near the tympanic membrane. (D) The ossicles are malformed, with underdeveloped and fused malleus and incus (arrow).
anomalous course of the facial nerve, small middle ear cavity, enlarged vestibular aqueduct, anomalous course of the vestibular aqueduct, small IAC (Figure 6), and presence of an anomalous emissary vein referred to as a petrosquamosal sinus.20
Branchio-oto-renal syndrome Branchio-oto-renal (BOR) is a relatively uncommon anomaly, with an estimated prevalence as high as 1:40,000,21
Figure 4 Congenital cholesteatoma in a patient with oculoauriculovertebral spectrum disorder. The left external auditory canal is atretic. An expansile, lucent lesion in the tympanic portion of the temporal bone (arrow), with well-defined scalloped edges, represents a congenital cholesteatoma.
though likely lower. However, its characteristic clinical and imaging features make it worthy of discussion here. BOR is an autosomal dominant disorder with variable penetrance, characterized by preauricular pits, “cup ear” deformity of the auricle, and renal anomalies ranging from mild hypoplasia to complete absence.22 Chang et al22 described “major” and “minor” features of BOR and proposed clinical criteria for diagnosis based on these features. When renal anomalies are absent, BOR is sometimes termed “branchiootic syndrome.” Hearing loss may be conductive, sensorineural, or mixed. Inner ear anomalies typically consist of incomplete formation of the cochlea, with only 2 turns, enlarged vestibular aqueduct, and bulbous IACs (Figure 7).23 Dysplasia of the LSC is also common.24 Middle ear anomalies typically involve the ossicles and include fusion of the malleus and incus, dysplastic or hypoplastic stapes, and fixation of the malleus to the anterior tympanic wall. Hypoplasia of the pyramidal eminence and atresia of the oval window have also been described.24
Vestibular and cochlear malformations Nonsyndromic vestibular and cochlear malformations exist along a spectrum, from complete labyrinthine aplasia
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Figure 5 CHARGE syndrome. MRI with axial cisternographic T2. (A and B) A small vestibule is identified (long arrows), without evidence of formation of the semicircular canals. (B and C) The cochlea (short arrows) is dysplastic, with a normally formed basal turn (C), but with incomplete formation of the middle and apical turns (B). (D) A coloboma is seen at the optic nerve head (double arrows). (E) 3D maximum-intensity projection T2 of the labyrinth showing dysplastic vestibule (long arrow) and dysplastic cochlea (short white arrow), as seen earlier. Atresia of the cochlear aperture (black arrow) reflects aplasia of the cochlear nerve. (F) Normal labyrinth in a different patient, showing the normal appearance of the internal auditory canal (IAC); cochlear aperture (CA); cochlea basal (B), middle (M), and apical (A) turns; vestibule (V); and semicircular canals.
(“Michel dysplasia”) on the most severe end to slight dysplasia of the cochlea or LSC on the mild end, depending on the time of the insult during embryologic development. The spectrum of cochlear anomalies (Figure 8) includes complete cochlear aplasia, cystic dysplasia without a
definable modiolus or cochlear turns (incomplete partitionI), and mild dysplasia with a well-defined basal turn but with fused middle and apical turns (ie, incomplete partition-II or classic Mondini dysplasia, Figures 1 and 2).25 Provided that there is a cochlear nerve, the latter 2 conditions can be treated with cochlear implantation.
Figure 6 CHARGE syndrome with complete vestibulocochlear nerve aplasia. MRI with axial cisternographic T2. (A) Image through the level of the IAC shows a small internal auditory canal (arrow), without definite nerves running through it or within the cerebellopontine angle cistern. (B) Image slightly lower shows normally formed cochlear turns but complete atresia of the cochlear aperture (arrow).
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Figure 7 Branchio-oto-renal syndrome (BOR). Axial CT. (A) Image through the level of the vestibule and lateral semicircular canal shows enlargement of the vestibular aqueduct at its midpoint (long arrow). (B) Image slightly lower shows enlargement of the external aperture of the vestibular aqueduct (long arrow). Cochlear dysplasia is also evident, with fusion of the middle and apical turns (short black arrow), that is, IP-II. (C) Ossicular dysplasia is relatively mild in this case. The malleus handle (short white arrow) is mildly dysplastic. The long process of the incus is also somewhat foreshortened; it should normally be seen on this image. IP, incomplete partition.
Figure 8 Spectrum of cochlear dysplasia. (A) Complete cochlear aplasia. Axial CT through the expected location of the cochlea (arrow) shows complete absence of the cochlea. (B) Common cavity. Axial CT shows a single compartment for both the vestibule and cochlea, without differentiation into separate structures (arrow). A cochlear implant lead is in place. (C and D) Incomplete partition type I (IP-I). (C) Axial CT and (D) coronal CT show a distinct cochlear bud (arrow) from the vestibule, without a definable modiolus or cochlear turns.
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clinical abnormalities: cholestasis, cardiac disease, skeletal abnormalities, ocular abnormalities, and a characteristic facial phenotype.29 Patients with LVAS and with cochlear malformations often respond well to cochlear implantation. The surgeon should be aware that there is an increased risk for CSF gusher and meningitis in these patients, as the malformation of the bony labyrinth leads to an abnormal communication between the CSF and the labyrinth (Figure 9).30
Cochlear nerve deficiency
Figure 9 CSF labyrinthine fistula. Coronal CT in a patient with incomplete cochlear partition shows abnormal accumulation of intrathecally administered contrast in the cochlea and vestibule (arrows).
The vestibule and semicircular canals develop concurrently with the cochlea, and as with the cochlea, the severity of the malformation depends on the time of the embryologic insult. The LSC is the last to develop. Therefore, when there is an isolated malformation of a single semicircular canal, it is invariably the lateral canal, which is fused with a cysticappearing vestibule. Earlier developmental insults result in malformation of the superior or PSCs or both. There are exceptions to this rule, such as isolated dysplasia of the PSC in Alagille syndrome and Waardenburg syndrome.26,27 Waardenburg syndrome is divided into 4 subtypes and is characterized primarily by abnormal pigmentation of the skin, hair, and iris.28 Alagille syndrome is an autosomal dominant disorder that traditionally has been defined by a paucity of intrahepatic bile ducts, in association with 5 main
CND is a commonly seen abnormality in the setting of SNHL. CND may be seen in association with syndromes, such as CHARGE, and is commonly seen in the setting of other cochlear and vestibular malformations. However, it may also be present as an isolated anomaly (Figure 10).31 On CT images, there may be narrowing of the cochlear aperture in the setting of CND. However, this finding can be insensitive and also difficult to detect.31 Specific measurements of the cochlear aperture width have been suggested, but it is our opinion that measurements are highly error prone, particularly when the abnormality is subtle, and we prefer a qualitative assessment. Narrowing of the IAC is also seen in many patients with CND,31,32 but this is also an insensitive finding. MRI is more effective than CT for detecting CND, especially in subtle cases, through direct demonstration of either absence or hypoplasia of the cochlear nerve on heavily T2-weighted cisternographic sequences. Oblique sagittal images are particularly helpful in demonstrating the cochlear nerve, which runs through the anterior and inferior quadrant of the IAC. When the cochlear nerve is hypoplastic, that is, smaller than the facial nerve, there is a poorer functional outcome from cochlear implantation compared with patients with a normal nerve.
Figure 10 Cochlear nerve deficiency. (A) Axial CT shows marked narrowing of the cochlear aperture (long black arrow) and narrowing of the internal auditory canal (white arrow). (B) Axial cisternographic T2 shows the same findings as (A) and also confirms absence of the vestibulocochlear nerve. Only a small facial nerve (short black arrow) is seen in the cerebellopontine angle. The normal vestibulocochlear nerve is typically thicker than the facial nerve and runs posterior to it.
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Absence of the vestibulocochlear nerve is a contraindication to cochlear implantation. These patients may be candidates for auditory brainstem implantation.
Summary A variety of congenital malformations of the ear may be encountered. Some of these malformations are part of welldescribed genetic syndromes, and in these cases CT and MRI are helpful in guiding clinical evaluation and establishing a diagnosis. In the setting of SNHL, CT and MRI play a critical role in establishing which patients are most likely to benefit from cochlear implantation.
References 1. Westerhof JP, Rademaker J, Weber BP, et al: Congenital malformations of the inner ear and the vestibulocochlear nerve in children with sensorineural hearing loss: Evaluation with CT and MRI. J Comput Assist Tomogr 25(5):719-726, 2001 2. Dewan K, Wippold FJ II, Lieu JEC: Enlarged vestibular aqueduct in pediatric sensorineural hearing loss. Otolaryngol Head Neck Surg 140(4):552-558, 2009 3. Valvassori GE, Clemis JD: The large vestibular aqueduct syndrome. Laryngoscope 88(5):723-728, 1978 4. Hill JH, Freint AJ, Mafee MF: Enlargement of the vestibular aqueduct. Am J Otolaryngol 5(6):411-414, 1984 5. Ma X, Yang Y, Xia M, et al: Computed tomography findings in large vestibular aqueduct syndrome. Acta Otolaryngol 129(7):700-708, 2009 6. Okamoto K, Ito J, Furusawa T, et al: MRI of enlarged endolymphatic sacs in the large vestibular aqueduct syndrome. Neuroradiology 40(3):167-172, 1998 7. Madden C, Halsted T, Benton T, et al: Enlarged vestibular aqueduct syndrome in the pediatric population. Otol Neurotol 24(4):625-632, 2003 8. Reardon W, OMahoney CF, Trembath R, et al: Enlarged vestibular aqueduct: A radiological marker of Pendred syndrome, and mutation of the PDS gene. QJM 93(2):99-104, 2000 9. Boston M, Halsted M, Meinzenderr J, et al: The large vestibular aqueduct: A new definition based on audiologic and computed tomography correlation. Otolaryngol Head Neck Surg 136(6):972-977, 2007 10. Welker KL, Orkin JD, Ryan TM: Analysis of intraindividual and intraspecific variation in semicircular canal dimensions using highresolution x-ray computed tomography. J Anat 215(4):444-451, 2009 11. Ozgen B, Cunnane ME, Caruso PA, et al: Comparison of 451 oblique reformats with axial reformats in CT evaluation of the vestibular aqueduct. Am J Neuroradiol 29(1):30-34, 2008 12. Rosa RFM, Silva APD, Goetze TB, et al: Ear abnormalities in patients with oculo-auriculo-vertebral spectrum (Goldenhar syndrome). Braz J Otorhinolaryngol 77(4):455-460, 2011
13. Birgfeld C, Heike C: Craniofacial microsomia. Semin Plast Surg 26(2):91-104, 2012 14. Mafee MF, Valvassori GE: Radiology of the craniofacial anomalies. Otolaryngol Clin North Am 14(4):939-988, 1981 15. Phelps PD, Lloyd GA, Poswillo DE: The ear deformities in craniofacial microsomia and oculo-auriculo-vertebral dysplasia. J Laryngol Otol 97(11):995-1005, 1983 16. Strömland K, Miller M, Sjögreen L, et al: Oculo-auriculo-vertebral spectrum: Associated anomalies, functional deficits and possible developmental risk factors. Am J Med Genet 143A(12):1317-1325, 2007 17. Jin L, Hao S, Fu Y, et al: Clinical analysis based on 208 patients with microtia (especially reviewed oculo-auriculo-vertebral spectrum, hearing test, CT scan). Turk J Pediatr 52(6):582-587, 2010 18. Kelley PE, Scholes MA: Microtia and congenital aural atresia. Otolaryngol Clin North Am 40(1):61-80, 2007 19. Blake KD, Prasad C: CHARGE syndrome. Orphanet J Rare Dis 1:34, 2006 20. Morimoto AK, Wiggins RHI, Hudgins PA, et al: Absent semicircular canals in CHARGE syndrome: Radiologic spectrum of findings. Am J Neuroradiol 27(8):1663-1671, 2006 21. Fraser FC, Sproule JR, Halal F: Frequency of the branchio-oto-renal (BOR) syndrome in children with profound hearing loss. Am J Med Genet 7(3):341-349, 1980 22. Chang EH, Menezes M, Meyer NC, et al: Branchio-oto-renal syndrome: The mutation spectrum in EYA1 and its phenotypic consequences. Hum Mutat 23(6):582-589, 2004 23. Chen A, Francis M, Ni L, et al: Phenotypic manifestations of branchiooto-renal syndrome. Am J Med Genet 58(4):365-370, 1995 24. Ceruti S, Stinckens C, Cremers C, et al: Temporal bone anomalies in the branchio-oto-renal syndrome: Detailed computed tomographic and magnetic resonance imaging findings. Otol Neurotol 23(2):200-207, 2002 25. Sennaroglu L, Saatci I: A new classification for cochleovestibular malformations. Laryngoscope 112(12):2230-2241, 2002 26. Koch B, Goold A, Egelhoff J, et al: Partial absence of the posterior semicircular canal in Alagille syndrome: CT findings. Pediatr Radiol 36(9):977-979, 2006 27. Mafee MF, Selis JE, Yannias DA, et al: Congenital sensorineural hearing loss. Radiology 150(2):427-434, 1984 28. Read AP, Newton VE: Waardenburg syndrome. J Med Genet 34(8): 656-665, 1997 29. Li L, Krantz ID, Deng Y, et al: Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet 16(3):243-251, 1997 30. Kim L-S, Jeong S-W, Huh M-J, et al: Cochlear implantation in children with inner ear malformations. Ann Otol Rhinol Laryngol 115(3): 205-214, 2006 31. Yan F, Li J, Xian J, et al: The cochlear nerve canal and internal auditory canal in children with normal cochlea but cochlear nerve deficiency. Acta Radiol 54(3):292-298, 2013 32. Glastonbury CM, Davidson HC, Harnsberger HR, et al: Imaging findings of cochlear nerve deficiency. Am J Neuroradiol 23(4): 635-643, 2002
Imaging of congenital temporal bone anomalies Ali R. Sepahdari, MD,a Brian D. Zipser, MD,b Michael N. Pakdaman, MDa From the aDepartment of Radiological Sciences, David Geffen SOM, University of California, Los Angeles, California; and the bDepartment of Radiology, Olive View Medical Center, Sylmar, California KEYWORDS Congenital temporal bone anomalies; Pediatric sensorineural hearing loss; Large vestibular aqueduct; CHARGE; Oculoauriculovertebral
A variety of congenital malformations of the ear and temporal bone may be encountered. Anomalies of the inner ear, middle ear, and external auditory canal and auricle can all occur, and there are a variety of clinical presentations that include conductive and sensorineural hearing loss. Some malformations are part of well-described genetic syndromes, whereas others are sporadic. Cochlear implantation may be helpful in some cases. Knowledge of typical patterns of abnormalities can help guide the clinical workup and management plan. The goal of this review is to familiarize the reader with the role of imaging in some of the commonly encountered congenital malformations of the ear and temporal bone. r 2014 Elsevier Inc. All rights reserved.
Introduction When evaluating the pediatric patient with hearing loss, imaging is essential before considering corrective surgery. Congenital anomalies of the temporal bone may produce conductive hearing loss (CHL) or sensorineural hearing loss (SNHL). Imaging is essential in determining whether a patient is likely to benefit from external middle ear corrective surgery in patients with CHL or from cochlear implantation in cases of SNHL and is essential also for guiding workup for a potential underlying genetic syndrome.
Imaging modalities Computed tomography (CT) and magnetic resonance imaging (MRI) are the 2 imaging modalities that are commonly used to evaluate the pediatric patient with hearing loss. Some centers use only 1 modality, whereas others (including our institution) often use both.1 We find CT and MRI to be complementary tests. CT is superior for Address reprint requests and correspondence: Ali R Sepahdari, MD, 757 Westwood Plaza, Suite 1621D, Los Angeles, CA 90095. E-mail address: [email protected]; [email protected] 1043-1810/$ - see front matter r 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.otot.2013.11.003
showing the middle ear anatomy, anomalies of the ossicular chain, and course of the facial nerve canal. Patency of the labyrinthine oval window and round window niche, volume of the middle ear cavity, and anatomical constraints to successful auriculotympano or ossiculoplasty and cochlear implantation are best seen by CT. CT and MRI are similarly sensitive for detecting malformations of the inner ear. Although CT can suggest cochlear nerve deficiency (CND) if the cochlear aperture or internal auditory canal (IAC) is small, MRI is superior in detecting CND through direct visualization of the nerve. Attention to detail is important in ensuring that diagnostic quality images are obtained for both CT and MRI. Close communication between the otologist and the radiologist is helpful in this regard. For CT, it is preferable to perform the studies on a newer model multidetector row scanner (eg, 64 detector row or higher), though high-quality images can still be obtained on older scanners, albeit at the cost of higher radiation dose. It is critical to obtain thinsection images reconstructed in a sharp bone algorithm with a small field of view, ideally with separate small field-ofview reconstructions of the right and left sides separately so as to maximize spatial resolution. With newer model scanners, a volumetric axial acquisition can be reconstructed in the axial and coronal planes and in oblique planes as needed. With older scanners, direct coronal imaging may be
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necessary. When performing MRI, it is of critical importance to obtain high-resolution, 3-dimensional (3D), heavily T2-weighted “cisternographic” sequences to visualize the vestibulocochlear nerves and the labyrinthine structures. These sequences have different names and acronyms according to the MRI manufacturer and the technique that is used to produce the image. Some examples include Constructive Interference in Steady State, Fast Imaging Employing Steady-state Acquisition, 3D DRIVen Equilibrium, T2 Sampling Perfection with Application-optimized Contrasts using different flip angle Evolutions, and Balanced Fast Field Echo. Close communication between the otologist and the radiologist can help ensure that a correct MRI protocol is performed. Sedation is typically required for MRI. CT can often be performed without sedation, particularly with newer scanners that are able to image the entire temporal bone in several seconds.
Syndromic anomalies A variety of genetic syndromes may lead to malformations of the external, middle, and inner ear. Hearing loss may be sensorineural, conductive, or mixed. Certain characteristic patterns of involvement have been described with these conditions, and temporal bone imaging can often guide the genetic workup.
Large vestibular aqueduct syndrome Enlargement of the vestibular aqueduct is the most commonly seen abnormality in pediatric SNHL.2 As this may be a feature of a variety of other syndromic and nonsyndromic malformations, the term large vestibular aqueduct syndrome (LVAS) is typically used to describe
this anomaly when it occurs in isolation or with incomplete cochlear partition (“Mondini” dysplasia) as the only other abnormality. LVAS was first described in 1978 by Valvassori and Clemis3 using polytomography, now an obsolete imaging modality, and later by Hill et al4 using CT. On CT, the characteristic abnormality is enlargement of the vestibular aqueduct (Figure 1). Incomplete cochlear partition (fusion of the middle and apical turns, with missing bony partition [osseous spiral lamina], ie, “Mondini” dysplasia) is a common associated finding, as is mild dysplasia of the lateral semicircular canal (LSC) with associated small LSC bone island.5 On magnetic resonance images, enlargement of both the endolymphatic duct and the endolymphatic sac are evident (Figure 2).6 The typical presentation is of SNHL of varying severity, which may be stable, progressive, or fluctuating.7 Sudden deterioration following trivial head trauma or minor ailments may also be seen.7 Pendred syndrome describes the syndrome of deafness and goiter. Patients with Pendred syndrome typically have abnormal results on perchlorate discharge tests and a mutation of the PDS gene and frequently show radiologic findings of enlarged vestibular aqueduct with incomplete cochlear partition. A recent study showed that many patients with enlarged vestibular aqueducts, but without goiter, have PDS gene mutations,8 suggesting that LVAS and Pendred syndrome lie along a common spectrum. Different criteria have been described for determining whether a vestibular aqueduct is enlarged. Some use an absolute diameter of more than 1.5 mm, measured on axial images at the midpoint between the isthmus and the external aperture, as the cutoff for a normal vestibular aqueduct, basing this on criteria determined from polytomography.3 Some have proposed using cutoffs of more than 0.9 mm at the midpoint or more than 1.9 mm at the external aperture (operculum), termed the “Cincinnati criteria.”2,9 Others
Figure 1 Large vestibular aqueduct syndrome. Axial CT. (A) Image through the level of the lateral semicircular canal shows gross enlargement of the vestibular aqueduct (long arrow). Compare with the posterior semicircular canal (short white arrow) in the same image. (B) Image slightly lower shows cochlear dysplasia with fusion of the middle and apical turns (ie, incomplete partition-II, a.k.a. Mondini dysplasia).
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Figure 2 Large vestibular aqueduct syndrome, same patient as Figure 1. (A) Axial cisternographic T2 MRI shows the same findings. Incomplete cochlear partition (short white arrow) and enlarged vestibular aqueduct (long white arrow) are again noted. Dilation of the endolymphatic sac (long black arrow) is also evident. (B) 3D maximum-intensity projection T2 of the labyrinth shows the dilated endolymphatic sac (ES) and endolymphatic duct (ED).
(including these authors) use the posterior semicircular canal (PSC) as an internal reference marker for size. The PSC, which is well seen at the level of the vestibular aqueduct midpoint, has a diameter of approximately 1.5 cm.10 Using this internal reference marker allows for visual comparison of multiple contiguous images. A measurement of greater than 1 mm at the isthmus of the vestibular aqueduct should also be considered abnormal. Ozgen et al11 noted that measurement of the vestibular aqueduct caliber was more consistent using 451 oblique reconstructions compared with standard axial plane images, though this observation has not resulted in the large-scale revision of criteria for vestibular aqueduct enlargement.
Oculoauricolovertebral spectrum (a.k.a. hemifacial microsomia, craniofacial microsomia, Goldenhar syndrome, and first and second branchial arch anomaly) Oculoauricolovertebral spectrum disorder is a rare, complex, and phenotypically variable birth defect involving the first and second branchial arch derivatives, with estimated prevalence between 1:5,600 and 1:26,650 live births.12 The highly variable phenotype of oculoauricolovertebral spectrum includes craniofacial anomalies and cardiac, vertebral, and central nervous system defects. Most cases are sporadic, but there are rare familial cases that exhibit autosomal dominant inheritance. These patients, unlike those with mandibulofacial dysostosis (Treacher Collins syndrome), typically exhibit an asymmetric deformity of the external ear, small mandible, and hypoplastic or frankly atretic external auditory canal (Figure 3). The severity of the external ear deformity is a basis on which the severity of disease is classified.13 Middle ear anomalies are commonly seen and well characterized.14,15 Inner ear anomalies are less common and include atresia of
the IAC and malformations of the cochlea and semicircular canals.12 CHL is almost always present, with mixed or sensorineural hearing loss being less common.16 Facial nerve palsy may also be seen. In addition to external auditory canal hypoplasia or atresia, which is typically clinically apparent, CT often reveals lateral displacement of the ossicles, malformation of the ossicular chain, low tegmen, and underdevelopment of the mastoid air cells (Figure 3).12,15,17 CT is critical in guiding surgery, as the mastoid segment of the facial nerve canal is typically superficial and more anterior than normal. At times, a congenital cholesteatoma may be present deep to the atretic external auditory canal or at the site of the dysplastic segment of the tympanic part of the temporal bone (Figure 4). CT is critical to detect these lesions, though they may not be detected if the CT is performed too early in life.18
CHARGE syndrome CHARGE syndrome is characterized by a variety of congenital anomalies, including those that compose its name (coloboma, heart anomalies, choanal atresia, mental retardation, genital hypoplasia, and ear anomalies), as well as facial palsy, cleft palate, esophageal atresia, facial dysmorphism, and CNS malformations (Online Mendelian Inheritance in Man, Entry no. 214800). Reports of its prevalence range from 0.2-1.2 every 10,000 live births.19 Major diagnostic criteria are the “4 Cs”: characteristic ear anomaly, coloboma, choanal atresia, and cranial nerve abnormality. The characteristic ear anomaly of CHARGE syndrome is aplasia or hypoplasia of the semicircular canals (Figure 5). Hypoplasia or aplasia of the cochlear nerve is also common in CHARGE syndrome,20 and it is essential to evaluate for this carefully if cochlear implantation is considered (Figures 5 and 6). Other abnormalities include oval or round window atresia or hypoplasia, ossicular dysplasia with ankylosis, cochlear dysplasia, dysplastic or hypoplastic vestibule,
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Figure 3 Oculoauriculovertebral spectrum, that is, Goldenhar syndrome. Coronal CT. (A and B) Normal coronal CT through the right ear. (C) The left external auditory canal is narrowed (arrow) and nearly atretic near the tympanic membrane. (D) The ossicles are malformed, with underdeveloped and fused malleus and incus (arrow).
anomalous course of the facial nerve, small middle ear cavity, enlarged vestibular aqueduct, anomalous course of the vestibular aqueduct, small IAC (Figure 6), and presence of an anomalous emissary vein referred to as a petrosquamosal sinus.20
Branchio-oto-renal syndrome Branchio-oto-renal (BOR) is a relatively uncommon anomaly, with an estimated prevalence as high as 1:40,000,21
Figure 4 Congenital cholesteatoma in a patient with oculoauriculovertebral spectrum disorder. The left external auditory canal is atretic. An expansile, lucent lesion in the tympanic portion of the temporal bone (arrow), with well-defined scalloped edges, represents a congenital cholesteatoma.
though likely lower. However, its characteristic clinical and imaging features make it worthy of discussion here. BOR is an autosomal dominant disorder with variable penetrance, characterized by preauricular pits, “cup ear” deformity of the auricle, and renal anomalies ranging from mild hypoplasia to complete absence.22 Chang et al22 described “major” and “minor” features of BOR and proposed clinical criteria for diagnosis based on these features. When renal anomalies are absent, BOR is sometimes termed “branchiootic syndrome.” Hearing loss may be conductive, sensorineural, or mixed. Inner ear anomalies typically consist of incomplete formation of the cochlea, with only 2 turns, enlarged vestibular aqueduct, and bulbous IACs (Figure 7).23 Dysplasia of the LSC is also common.24 Middle ear anomalies typically involve the ossicles and include fusion of the malleus and incus, dysplastic or hypoplastic stapes, and fixation of the malleus to the anterior tympanic wall. Hypoplasia of the pyramidal eminence and atresia of the oval window have also been described.24
Vestibular and cochlear malformations Nonsyndromic vestibular and cochlear malformations exist along a spectrum, from complete labyrinthine aplasia
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Figure 5 CHARGE syndrome. MRI with axial cisternographic T2. (A and B) A small vestibule is identified (long arrows), without evidence of formation of the semicircular canals. (B and C) The cochlea (short arrows) is dysplastic, with a normally formed basal turn (C), but with incomplete formation of the middle and apical turns (B). (D) A coloboma is seen at the optic nerve head (double arrows). (E) 3D maximum-intensity projection T2 of the labyrinth showing dysplastic vestibule (long arrow) and dysplastic cochlea (short white arrow), as seen earlier. Atresia of the cochlear aperture (black arrow) reflects aplasia of the cochlear nerve. (F) Normal labyrinth in a different patient, showing the normal appearance of the internal auditory canal (IAC); cochlear aperture (CA); cochlea basal (B), middle (M), and apical (A) turns; vestibule (V); and semicircular canals.
(“Michel dysplasia”) on the most severe end to slight dysplasia of the cochlea or LSC on the mild end, depending on the time of the insult during embryologic development. The spectrum of cochlear anomalies (Figure 8) includes complete cochlear aplasia, cystic dysplasia without a
definable modiolus or cochlear turns (incomplete partitionI), and mild dysplasia with a well-defined basal turn but with fused middle and apical turns (ie, incomplete partition-II or classic Mondini dysplasia, Figures 1 and 2).25 Provided that there is a cochlear nerve, the latter 2 conditions can be treated with cochlear implantation.
Figure 6 CHARGE syndrome with complete vestibulocochlear nerve aplasia. MRI with axial cisternographic T2. (A) Image through the level of the IAC shows a small internal auditory canal (arrow), without definite nerves running through it or within the cerebellopontine angle cistern. (B) Image slightly lower shows normally formed cochlear turns but complete atresia of the cochlear aperture (arrow).
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Figure 7 Branchio-oto-renal syndrome (BOR). Axial CT. (A) Image through the level of the vestibule and lateral semicircular canal shows enlargement of the vestibular aqueduct at its midpoint (long arrow). (B) Image slightly lower shows enlargement of the external aperture of the vestibular aqueduct (long arrow). Cochlear dysplasia is also evident, with fusion of the middle and apical turns (short black arrow), that is, IP-II. (C) Ossicular dysplasia is relatively mild in this case. The malleus handle (short white arrow) is mildly dysplastic. The long process of the incus is also somewhat foreshortened; it should normally be seen on this image. IP, incomplete partition.
Figure 8 Spectrum of cochlear dysplasia. (A) Complete cochlear aplasia. Axial CT through the expected location of the cochlea (arrow) shows complete absence of the cochlea. (B) Common cavity. Axial CT shows a single compartment for both the vestibule and cochlea, without differentiation into separate structures (arrow). A cochlear implant lead is in place. (C and D) Incomplete partition type I (IP-I). (C) Axial CT and (D) coronal CT show a distinct cochlear bud (arrow) from the vestibule, without a definable modiolus or cochlear turns.
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clinical abnormalities: cholestasis, cardiac disease, skeletal abnormalities, ocular abnormalities, and a characteristic facial phenotype.29 Patients with LVAS and with cochlear malformations often respond well to cochlear implantation. The surgeon should be aware that there is an increased risk for CSF gusher and meningitis in these patients, as the malformation of the bony labyrinth leads to an abnormal communication between the CSF and the labyrinth (Figure 9).30
Cochlear nerve deficiency
Figure 9 CSF labyrinthine fistula. Coronal CT in a patient with incomplete cochlear partition shows abnormal accumulation of intrathecally administered contrast in the cochlea and vestibule (arrows).
The vestibule and semicircular canals develop concurrently with the cochlea, and as with the cochlea, the severity of the malformation depends on the time of the embryologic insult. The LSC is the last to develop. Therefore, when there is an isolated malformation of a single semicircular canal, it is invariably the lateral canal, which is fused with a cysticappearing vestibule. Earlier developmental insults result in malformation of the superior or PSCs or both. There are exceptions to this rule, such as isolated dysplasia of the PSC in Alagille syndrome and Waardenburg syndrome.26,27 Waardenburg syndrome is divided into 4 subtypes and is characterized primarily by abnormal pigmentation of the skin, hair, and iris.28 Alagille syndrome is an autosomal dominant disorder that traditionally has been defined by a paucity of intrahepatic bile ducts, in association with 5 main
CND is a commonly seen abnormality in the setting of SNHL. CND may be seen in association with syndromes, such as CHARGE, and is commonly seen in the setting of other cochlear and vestibular malformations. However, it may also be present as an isolated anomaly (Figure 10).31 On CT images, there may be narrowing of the cochlear aperture in the setting of CND. However, this finding can be insensitive and also difficult to detect.31 Specific measurements of the cochlear aperture width have been suggested, but it is our opinion that measurements are highly error prone, particularly when the abnormality is subtle, and we prefer a qualitative assessment. Narrowing of the IAC is also seen in many patients with CND,31,32 but this is also an insensitive finding. MRI is more effective than CT for detecting CND, especially in subtle cases, through direct demonstration of either absence or hypoplasia of the cochlear nerve on heavily T2-weighted cisternographic sequences. Oblique sagittal images are particularly helpful in demonstrating the cochlear nerve, which runs through the anterior and inferior quadrant of the IAC. When the cochlear nerve is hypoplastic, that is, smaller than the facial nerve, there is a poorer functional outcome from cochlear implantation compared with patients with a normal nerve.
Figure 10 Cochlear nerve deficiency. (A) Axial CT shows marked narrowing of the cochlear aperture (long black arrow) and narrowing of the internal auditory canal (white arrow). (B) Axial cisternographic T2 shows the same findings as (A) and also confirms absence of the vestibulocochlear nerve. Only a small facial nerve (short black arrow) is seen in the cerebellopontine angle. The normal vestibulocochlear nerve is typically thicker than the facial nerve and runs posterior to it.
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Absence of the vestibulocochlear nerve is a contraindication to cochlear implantation. These patients may be candidates for auditory brainstem implantation.
Summary A variety of congenital malformations of the ear may be encountered. Some of these malformations are part of welldescribed genetic syndromes, and in these cases CT and MRI are helpful in guiding clinical evaluation and establishing a diagnosis. In the setting of SNHL, CT and MRI play a critical role in establishing which patients are most likely to benefit from cochlear implantation.
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13. Birgfeld C, Heike C: Craniofacial microsomia. Semin Plast Surg 26(2):91-104, 2012 14. Mafee MF, Valvassori GE: Radiology of the craniofacial anomalies. Otolaryngol Clin North Am 14(4):939-988, 1981 15. Phelps PD, Lloyd GA, Poswillo DE: The ear deformities in craniofacial microsomia and oculo-auriculo-vertebral dysplasia. J Laryngol Otol 97(11):995-1005, 1983 16. Strömland K, Miller M, Sjögreen L, et al: Oculo-auriculo-vertebral spectrum: Associated anomalies, functional deficits and possible developmental risk factors. Am J Med Genet 143A(12):1317-1325, 2007 17. Jin L, Hao S, Fu Y, et al: Clinical analysis based on 208 patients with microtia (especially reviewed oculo-auriculo-vertebral spectrum, hearing test, CT scan). Turk J Pediatr 52(6):582-587, 2010 18. Kelley PE, Scholes MA: Microtia and congenital aural atresia. Otolaryngol Clin North Am 40(1):61-80, 2007 19. Blake KD, Prasad C: CHARGE syndrome. Orphanet J Rare Dis 1:34, 2006 20. Morimoto AK, Wiggins RHI, Hudgins PA, et al: Absent semicircular canals in CHARGE syndrome: Radiologic spectrum of findings. Am J Neuroradiol 27(8):1663-1671, 2006 21. Fraser FC, Sproule JR, Halal F: Frequency of the branchio-oto-renal (BOR) syndrome in children with profound hearing loss. Am J Med Genet 7(3):341-349, 1980 22. Chang EH, Menezes M, Meyer NC, et al: Branchio-oto-renal syndrome: The mutation spectrum in EYA1 and its phenotypic consequences. Hum Mutat 23(6):582-589, 2004 23. Chen A, Francis M, Ni L, et al: Phenotypic manifestations of branchiooto-renal syndrome. Am J Med Genet 58(4):365-370, 1995 24. Ceruti S, Stinckens C, Cremers C, et al: Temporal bone anomalies in the branchio-oto-renal syndrome: Detailed computed tomographic and magnetic resonance imaging findings. Otol Neurotol 23(2):200-207, 2002 25. Sennaroglu L, Saatci I: A new classification for cochleovestibular malformations. Laryngoscope 112(12):2230-2241, 2002 26. Koch B, Goold A, Egelhoff J, et al: Partial absence of the posterior semicircular canal in Alagille syndrome: CT findings. Pediatr Radiol 36(9):977-979, 2006 27. Mafee MF, Selis JE, Yannias DA, et al: Congenital sensorineural hearing loss. Radiology 150(2):427-434, 1984 28. Read AP, Newton VE: Waardenburg syndrome. J Med Genet 34(8): 656-665, 1997 29. Li L, Krantz ID, Deng Y, et al: Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet 16(3):243-251, 1997 30. Kim L-S, Jeong S-W, Huh M-J, et al: Cochlear implantation in children with inner ear malformations. Ann Otol Rhinol Laryngol 115(3): 205-214, 2006 31. Yan F, Li J, Xian J, et al: The cochlear nerve canal and internal auditory canal in children with normal cochlea but cochlear nerve deficiency. Acta Radiol 54(3):292-298, 2013 32. Glastonbury CM, Davidson HC, Harnsberger HR, et al: Imaging findings of cochlear nerve deficiency. Am J Neuroradiol 23(4): 635-643, 2002