|Year : 2016 | Volume
| Issue : 4 | Page : 248-257
Evaluation of embryological sequences of ear anomalies and its radiological relevance
C Amarnath, G Sathyan, R Soniya, AL Periakaruppan, K Shiva Shankar
Department of Radiodiagnosis, Stanley Medical College, Chennai, Tamil Nadu, India
|Date of Web Publication||13-Oct-2016|
Department of Radiodiagnosis, Stanley Medical College, Chennai - 600 001, Tamil Nadu
Source of Support: None, Conflict of Interest: None
Aim: To correlate the sequence of embryological development of ear with radiological imaging. Materials and Methods: The study enrolled 23 patients of age group 11 months to 27 years with malformed external ear/microtia and hearing loss. The children with postoperative changes, acute hearing loss (such as infection, trauma) were excluded from the study. We used high-resolution computed tomography, with axial and coronal sections to examine the temporal bones of patients. Results: Of the 23 cases, 12 cases had external ear anomaly and 11 cases had cochlear anomaly. In patients with the external ear anomaly, seven cases had associated middle ear malformations, one patient had associated middle and inner ear anomaly, one had anomalous course of facial nerve, and three cases had isolated external ear anomalies. In patients with inner ear anomalies, one patient had complete labyrinthine aplasia, one had cochlear dysplasia with incomplete cochlear turns, four had common cavity malformations, one had cystic featureless cochlea with dilated and cystic vestibule, two patients had small cochlea with the middle and apical turns coalescing to form a cystic apex, one patient had small rudimentary cochlea, and the other one had dilated vestibule and enlarged endolymphatic duct and sac with cochlear dysmorphism. Conclusion: Most of the children with malformed pinna had external auditory canal atresia with associated middle ear anomalies. Though the inner ear development is independent of external and middle ear development, we insist on the fact that insult during the 1 st month of embryogenesis can result in associated abnormalities involving external, middle, and inner ear. Developmental arrest at various stages of inner ear development results in various types of cochlear anomalies with associated vestibular, semicircular canal abnormalities, and rarely associated with middle and external ear anomalies. Hence, clear knowledge about embryology will help to guide the management.
Keywords: Cochlea, Developmental arrest, External auditory canal, High-resolution computed tomography, Temporal bone
|How to cite this article:|
Amarnath C, Sathyan G, Soniya R, Periakaruppan A L, Shankar K S. Evaluation of embryological sequences of ear anomalies and its radiological relevance. Indian J Otol 2016;22:248-57
|How to cite this URL:|
Amarnath C, Sathyan G, Soniya R, Periakaruppan A L, Shankar K S. Evaluation of embryological sequences of ear anomalies and its radiological relevance. Indian J Otol [serial online] 2016 [cited 2021 Aug 1];22:248-57. Available from: https://www.indianjotol.org/text.asp?2016/22/4/248/192171
| Introduction|| |
This study gives a brief overview of congenital external and inner ear abnormalities. Here, we describe 23 cases of congenital external ear anomalies and inner ear anomalies and their correlation with developmental arrest during embryogenesis. Surgery for external auditory canal (EAC) atresia can be done between the ages of 5 and 7 years. Middle ear ossicles should be preserved if they are mobile and functional. If there are fused and nonfunctioning ossicles, it should be removed. The graft is then laid on the mobile stapes or footplate. Anomalous course of facial nerve is more common in these patients, so it should be notified to avoid the complications during surgery.  Cochlear implantation is preferred for most of the inner ear malformations which is contraindicated in case of complete labyrinthine aplasia and cochlear nerve deficiency.  Understanding the congenital abnormalities of the external, middle, and inner ear, with background knowledge on otogenesis guides the clinician in better patient management thereby achieving good prognosis. This article discusses about the normal embryology and developmental arrest of ear in various stages and its radiological correlation.
| Materials and Methods|| |
The study enrolled 23 patients of age group 11 months to 27 years with malformed external ear and hearing loss. The children with postoperative changes, acute hearing loss (like infection, trauma) were excluded from the study. Institutional Review Board approval for this study and informed consent were obtained.
High-resolution computed tomography (HRCT) scans are performed on a 6-slice volume CT scanner (Siemens, Germany) in a straight axial plane (matrix: 512 × 512, slice thickness: 0.625 mm, scan field of view [FOV]: 32 cm, display FOV: 9.6 cm). The original isometric volume data is used to obtain coronal reformatted images with slice thickness: 1.25 mm. The images are reviewed in a high-resolution bone algorithm, using a small FOV for separate right and left ear. Axial images are obtained from the petrous apex to the inferior tip of the mastoid bone. Reformatted coronal images are obtained from the anterior margin of the petrous apex to the posterior margin of the mastoid. Images are reviewed by a senior radiologist with 15 years of experience.
| Results|| |
In the observed 23 patients, 12 patients had EAC atresia and 11 had isolated inner ear anomalies. Of the 12 with EAC atresia, 7 patients (4 males and 3 females) had right sided anomaly, 4 patients (3 males and 1 female) had left sided anomaly, and 1 patient (male) with bilateral anomalies. In total, four patients had isolated external ear anomaly (17.4%), seven patients had associated middle ear involvement (30.4%), which includes ossicular involvement in six patients and involvement of both ossicles and facial nerve seen in one patient, one had all three external, middle, and inner ear anomaly (4.3%), and eleven patients (47.8%) had isolated inner ear anomaly. In the six patients with ossicular anomalies, four had dysplastic malleus and incus, two had fused malleus and incus, and one had ossicular disruption. Of the eleven with isolated inner ear anomaly, six (four females and two males) had left sided, three (males) had right sided, and two (one male and one female) had bilateral anomalies. In those patients, one patient had complete labyrinthine aplasia (9.1%), one had cochlear dysplasia with incomplete cochlear turns (9.1%), four had common cavity malformations (36.4%), one had cystic featureless cochlea with dilated and cystic vestibule (9.1%), two patients had small cochlea with the middle and apical turns coalescing to form a cystic apex (18.1%), one patient had small rudimentary cochlea (9.1%), and the other one had dilated vestibule and enlarged endolymphatic duct and sac with cochlear dysmorphism (9.1%). Patient characteristic and radiological feature are shown in [Table 1].
Case distribution features are shown in [Table 2] and [Table 3].
| Discussion|| |
Around the 3 rd week of gestation, the first evidence of inner ear development is seen as thickening of the ectoderm, on each side of the cephalic end. This aggregation of cells called the auditory or otic placode is preordained to become the membranous labyrinth. The otic placode invaginates inward to form the auditory or otic pit [Figure 1]a. The pit soon closes by itself in the 4 th week to form the auditory vesicle or otocyst [Figure 1]b. The otocyst migrates inward and the vestibular portion takes configuration slightly earlier than the cochlear portion. By the end of 5 weeks, the vestibular and cochlear divisions/pouches of the labyrinth [Figure 1]c-e are apparent and by 6 th week, the cochlea started forming by elongation of anterior aspect of cochlear pouch. The cochlea obtains nearly adult form by 10 weeks. Differentiation of the organ of Corti begins in the 10 th week [Figure 1]f. Around 11 weeks, there is a thickening of epithelium in the cochlear duct. From the 3 rd to 5 th month, this thickening differentiates into the distinct receptor and support cells of the organ of Corti. Meanwhile, the labyrinth continues to expand rapidly, so that near the end of the 5 th month, it is close to adult size. Thus, the cochlea is full sized and basically equipped in a span of 6 months. 
|Figure 1: Schematic representation of development of inner ear; (a) formation of otic pit by invagination of otic placode in 3½ week's embryo. (b) Otic pit completely closed by itself and otic vesicle formed by 4 weeks of embryonic life, (c and d) formation of the vestibular and cochlear divisions of the labyrinth by 4-5 weeks of embryonic life. (e) Formation of cochlea by elongation of anterior aspect of cochlear pouch and semicircular canal from utricular portion by 6-7th week. (f) Formation of well-formed membranous labyrinth by 8th week|
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The development of the vestibulo cochlear nerve and of the central auditory system is equally important but less understood. Ganglion cells from the eighth nerve arise from the otic vesicle in the 4 th gestational week. These fibers start to enter the expanding cochlea in the 5 th week. Afterward, the cochlear branch of the eighth nerve fans out in synchrony with the curving cochlea. Radial dendrites make contact with inner hair cells in 11 and 12 weeks, whereas spiral fibers contact the base of the outer hair cells in 14 th week. Efferent innervation is generally later than afferent innervation with axonic connections occurring between 15 and 22 weeks. All synapses are formed by the 7 th fetal month, and maturation of contact between the cochlea and peripheral nerves take place in the last trimester. As we have seen, though the organ of Corti is well formed in the 5 th month and synapses are forming in between 4 and 6 months, the sensorineural system is sufficiently mature to permit experiencing the sensation of sound near the end of the 6 th or start of the 7 th month.  The internal auditory canal (IAC) formed by inhibition of cartilage formation at the medial aspect of the otic vesicle. This inhibition requires the presence of the vestibulocochlear nerve. In the absence of the eighth nerve, IAC will not be formed. 
The middle ear development was first evidenced during the 4 th week. The first pharyngeal pouch extend lateral ward to form the tubotympanic recess, the primordium of the Eustachian tube More Details and the tympanic cavity [Figure 2]a and b. By 5 and 6 weeks, the mesenchymal cells lying in between the embryonic inner ear and the first branchial groove on the surface begin to show areas of concentration, which destined to become the ossicles. At nearly the same time, that same first branchial groove widens and extends inward to become the external auditory meatus. The first branchial arch forms the head and neck of the malleus and the body of the incus, whereas the handle of the malleus, the long process of the incus, and the head and crura of the stapes originate from the second branchial arch [Figure 2]c and d.  The stapes develops between the 5 th and 6 th week of gestational age, with its origins from the second branchial arch.  The footplate has a double origin, the lateral surface formed from the second arch and the medial surface from the otic capsule.  Between the 7 th and 9 th week, a depression emerges in the otic capsule, deep to the stapes footplate, in the future site of the oval window. The facial nerve, originating from the otic capsule and from second branchial arch, develops in a temporal window identical to the stapes. The failure of fusion of the two structures can lead to an anomalous facial nerve.  The orientation of facial nerve within the temporal bone has been established by the 8 th week, and the nerve's ultimate position and bony covering determined by development of the stapes and membranous labyrinth.  For much of their developmental time, the ossicles surrounded by mesenchymal tissue and not contained in a middle ear space. During 3 rd to 7 th month, this tissue resorbs, resulting in a marked expansion of the tympanic space to provide housing for the ossicles. 
|Figure 2: Schematic representation of stages in the formation of external and middle ear; (a) relationship of first pharyngeal groove with first pharyngeal pouch by 4th week. (b) Formation of middle ear ossicles from first to second pharyngeal arch by 5th week. (c) Meatal plug filling the deep portion of external auditory canal at 8-10 weeks of age. (d) Formation of external auditory canal by canalization of meatal plug at 13-18th weeks of age|
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The external ear was the last part to develop embryologically. By the end of 4 th week of gestation; four pairs of pharyngeal arches are externally visible in the neck region of embryo. The first two of these, the mandibular and hyoid arches, are important contributors to external ear development. During the 5 th gestational week, six nodular swellings of tissue known as the hillocks of His appear on the first and second pharyngeal arches.  By day 37, the pinna is well formed from these hillocks of His. It will be 4 months before the pinna has essentially adult form, although it continues to grow until the age of 9 years.  A short time after the appearance of the hillocks of His on the first and second branchial arches, the dorsal portion of the first pharyngeal cleft deepens to form a funnel-shaped depression that is the precursor of the EAC. At 4-5 weeks gestation, the primitive external canal establishes contact with the first pharyngeal pouch. In the 8 th week, the developing external canal deepens further to approach the middle ear space. Shortly thereafter, the ectodermal lining of the deep part of the primitive ear canal proliferates to form the meatal plug, which fills the medial portion of the canal. The meatal plate end in a rounded, disc-shaped swelling that lies immediately adjacent to the middle ear cavity. Continued canalization of the meatal plug produces the medial two-third of the definitive EAC. The meatal plug begins to open during the 13 th week of gestation and that the external canal is fully patent throughout its entire length in the 18 week fetus. The innermost portion of the meatal plate becomes the outer layer of the tympanic membrane.  The tympanic membrane trebles its diameter during 11-16 weeks, and its shape is completed by 19 th week. The membrane manifests its triple origins-on the inner side, a mucosal layer from endoderm, on the outer side, skin from ectoderm, and "sandwiched" in between, an elastic, fibrous layer from mesoderm. Its destined degree of verticality and curvature are reached by the age of 3 years. 
Anomalies of the ear
The embryology of the ear has implications in certain ear disorders. Since all the three germ cell tissues are in close proximity and the mesenchyme is involved in the development of all parts of the ear, combined malformations can occur in certain situations. Because of their more similar origins from the first to second branchial arches, outer and middle ear disorders are far more likely to coexist. The development of inner ear is independent of external and middle ear development, so it is less likely to coexist.  The timing of insults to the developing fetus holds a great influence on the extent of the disorder. Earlier the insult, more extensive is the anomaly. Depending on where the impact occurs, insults during early gestation would result in a rudimentary external, middle, or inner ear. In contrast, insults after 6 th month of gestation have little effect on these structures. 
Isolated inner ear anomaly
During otogenesis, developmental abnormalities that affect the otic capsule in specific time result in anomalies of both the bony and membranous labyrinth of different types. ,,
Michel's deformity (complete labyrinthine aplasia)
In the evaluated 23 patients, eleven patients presented with sensorineural hearing loss, in whom isolated inner ear anomaly was seen. Of the eleven patients, one patient (9.1%) had Michel's anomaly which is proposed to occur due to the arrest of otic placode early in the 3 rd week of gestational age.  It is very rare and seen in 1% of cases.  Cochlear implantation is contraindicated in Michel's aplasia, and auditory brainstem implantation may be considered as an option [Figure 3]. 
|Figure 3: High-resolution computed tomography temporal bone in 6-year-old girl. Three-dimensional reconstructed image showing complete labyrinthine aplasia (arrow) - absence of cochlea, semicircular canals on left side|
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Cochlear dysplasia is seen in one of our patients (9.1%). The arrest of otic placode, late in the 3 rd week of gestational age results in complete absence of Cochlea or cochlear dysplasia.  Vestibule and semicircular canals may be normal or malformed in these patients. It is seen in 3% of cases.  Cochlear implantation is the treatment of choice [Figure 4]a-c.  The electrode array was inserted into the vestibule through an oval window after removing the stapes or through a transmastoid labyrinthectomy site. 
|Figure 4: High-resolution computed tomography temporal bone in 4-year-old boy. (a and b) Multiplanar reconstructed images showing bilateral cochlear dysplasia (arrow) with incomplete cochlear turns. (c) Pictorial representation of cochlear anomaly (in embryo)-cochlear aplasia|
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Common cavity deformity
Common cavity malformation is seen in 4 (36.4) of our patients. It occurs due to arrest of otic placode during 4 th week of gestational age. There is no differentiation between the cochlea and the vestibule, both together forming a large cystic cavity with no internal architecture. One-fourth of all cochlear anomalies are common cavity malformations.  Semicircular canals frequently malformed or occasionally may be normal.  Since the exact location and amount of neural tissue are not definitely known, the surgeon uses full-banded implants with the use of a precurved electrode to avoid the risk of the electrode entering the IAC. These patients are at high risk for an intraoperative cerebrospinal fluid (CSF) gusher or postoperative CSF leak because they usually have a thin or absent cribriform area between the IAC and the common cavity [Figure 5]a and b. 
|Figure 5: High-resolution computed tomography temporal bone in 8-year-old boy. (a) Axial image showing common cavity malformation (arrow) on left side. (b) Pictorial representation of cochlear anomaly (in embryo)-common cavity malformation|
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Incomplete partition Type 1
It is otherwise called cystic cochleovestibular anomaly and it is seen in one (9.1%) of our patient. It occurs due to arrest of otic placode during 5 th week of gestational age. Because of lack of the entire modiolus, cochlea appears cystic, along with a large cystic vestibule giving "figure of eight" appearance.  The vestibule is distinguishable from the cochlea makes it possible to differentiate it from a common cavity malformation [Figure 6]a and b.  Cochlear implantation can be done for these patients but straight arrays with circumferential electrodes are preferred to stimulate as much neural tissue as possible. 
|Figure 6: High-resolution computed tomography temporal bone in 27-year-old man. (a) Coronal image showing cystic cochleo vestibular anomaly (arrow) on right side - cochlea and vestibule show "Figure 8" contour with no internal features. (b) Pictorial representation of cochlear anomaly (in embryo) - Incomplete partition Type 1|
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It occurs due to the arrest of otic placode during 6 th week of gestational age. In our study, one patient (9.1%) had cochlear hypoplasia constitutes a small rudimentary cochlea. They have normal or malformed vestibule and semicircular canals.  In these patients, if a full insertion is attempted, the electrode may enter the IAC due to the lack of space because the small space does not allow the electrode to curl within the cavity. Postoperative CSF leak is the main complication [Figure 7]. 
|Figure 7: Pictorial representation of cochlear anomaly (in embryo) - Cochlear hypoplasia|
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Mondini deformity (incomplete partition Type 2)
It occurs due to the arrest of otic placode during 7 th week of gestational age.  This malformation is seen in 2 (18.1%) of our patients, constitutes a small cochlea having basilar turn (1.5 turns), with the middle and apical turns coalescing to form a cystic apex. This deformity constitutes for the most common form of genetic deafness accounting for more than 50%.  The vestibule and semicircular canals may be normal with associated dilatation of the vestibule and vestibular aqueduct.  In those patients, if the modiolus and the basal turn are present, the surgical approach is similar to the one used in normal cases.  Main complication in these patients is postoperative CSF leak.[Figure 8]. Embryo-radiology of inner ear anomalies is shown in [Table 4].
|Figure 8: Pictorial representation of cochlear anomaly (in embryo) - Incomplete partition Type 2|
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Enlargement of the vestibular aqueduct
One of our patients (9.1%) had dilated vestibule and enlarged endolymphatic duct and sac with cochlear dysmorphism. The size of the mid portion of the vestibular aqueduct is >1.5 mm (measured at the midpoint of the common crus and external aperture), or its diameter is larger than that of the semicircular canal. It occurs due to insult in endolymphatic duct during 5-6 th weeks of gestational age. It is usually bilateral. In many cases, enlargement of vestibular aqueduct accompanies deformity of the other inner ear structures. An enlarged vestibular aqueduct is frequently seen in Pendred syndrome [Figure 9]a and b.  Hearing aids are beneficial in the event of fluctuating or progressive hearing loss. A cochlear implant is a viable option if hearing loss becomes profound. 
|Figure 9: High-resolution computed tomography temporal bone in 7-year-old girl. (a and b) Axial images showing dilated vestibule and enlarged vestibular aqueduct (arrow) with cochlear dysmorphism on bilateral side|
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Isolated external ear anomaly
In our study, twelve patients had malformed pinna. Of the 12 patients, 4 patients (17.4%) had isolated external ear anomaly. It occurs due to any insults that affect the first branchial groove during 4-13 th week of gestational age. 
External and middle ear anomalies
Seven patients (30.4%) had associated middle ear and external ear abnormalities. This is due to the insult that affected the first and second branchial arches during 5-6 th week of gestational age.  In the seven patients with associated middle and external ear anomalies, four were having dysplastic malleus and incus, two were having fused malleus and incus, and one patient had ossicular disruption. Abnormalities of the stapes are less common because of its dual origin from the second branchial arch and the otic capsule. In patients with EAC anomaly, the facial nerve canal had an anomalous course.  In our study, one patient had anomalous descending facial nerve canal which was noted within posterior aspect of bony septum of external auditory atresia.
Isolated middle ear anomaly
Though isolated middle ear anomalies are not uncommon, it is not seen in our patients. Most common isolated ossicular anomaly involves stapes, oval window, and facial nerve because their developments are closely related. 
External, middle and inner ear anomalies
One of our patients (4.3%) had all three external, middle, and inner ear anomalies. It occurred due to insult during the first 4 weeks of gestational age [Figure 10]a-i. 
|Figure 10: High-resolution computed tomography temporal bone. (a) Axial image showing right external auditory canal atresia (arrow) in an 18-year-old female. (b) Axial image in a 1-year-oldboy showing external auditory canal atresia (arrow) of mixed bony and soft tissue on left side with dysplastic malleus and incus (arrowhead). (c) Axial image in the same patient shows descending facial nerve canal (arrow) noted within posterior aspect of bony septum of external auditory atresia. (d) Axial image showing bilateral mixed bony and soft tissue external auditory canal atresia (arrow) with dysplastic malleus and incus in 4-year-old boy. (e) Coronal image showing right bony external auditory canal atresia (arrow) in a 4-year-old boy. (f) Axial image showing left external auditory canal atresia (arrow) including the bony and membranous portion in a 2-year-old male and (g) Axial image shows fusion of malleus and incus (arrow) in the same patient. (h) Coronal image showing right external auditory canal atresia (arrow) of mixed bony and soft tissue with dysplastic malleus and incus (arrowhead) in an 11-month-old male. (i) Coronal image showing, right external auditory canal atresia (arrow) involving both membranous and bony portions in a 5-year-old female|
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Embryo-radiology of external and middle ear anomalies is shown in [Table 5].
| Conclusion|| |
Malformed pinna is the most common ear anomaly and is frequently associated with external and middle ear anomalies because of common embryological origin. Depending upon the severity of external ear malformation/microtia and the time of insult during otogenesis, inner ear anomalies rarely may coexist with it. Various anomalies that involve both bony and the membranous labyrinth have been identified in children with sensory neural hearing loss. Most of such deformities manifest depending upon the gestational age at which the insult or arrest occurred. Surgery can be done for EAC between the ages of 5 and 7 years. Note must be given regarding the anomalous course of facial nerve to avoid the complications during surgery and about the ossicles status. Cochlear implantation is preferred for most of the inner ear malformations. Understanding the congenital abnormalities of the external, middle, and inner ear, with background knowledge on otogenesis guides the clinician in better patient management and to assess the prognosis.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]