[Skip to Content]
Access to paid content on this site is currently suspended due to excessive activity being detected from your IP address 23.23.50.247. Please contact the publisher to request reinstatement.
[Skip to Content Landing]
Download PDF
Coronal computed tomographic (CT) images and surgical view of temporal bones in a patient with external auditory canal (EAC) atresia (A and B) and stenosis (C and D). A, Surgical view of the right ear with EAC atresia. B, Axial CT image of the ear shown in A. C, Surgical view of the right ear with EAC stenosis. D, Coronal CT image of the ear shown in C. M indicates malleus; I, incus; H, manubrium; C, chorda tympani; and S, stapes.

Coronal computed tomographic (CT) images and surgical view of temporal bones in a patient with external auditory canal (EAC) atresia (A and B) and stenosis (C and D). A, Surgical view of the right ear with EAC atresia. B, Axial CT image of the ear shown in A. C, Surgical view of the right ear with EAC stenosis. D, Coronal CT image of the ear shown in C. M indicates malleus; I, incus; H, manubrium; C, chorda tympani; and S, stapes.

Table 1.  
Classification of 55 Ears With External Ear Canal Anomalies According to Schuknecht's Criteria3
Classification of 55 Ears With External Ear Canal Anomalies According to Schuknecht's Criteria3
Table 2.  
Relationship Between the Type of External Ear Canal Anomaly and Grade of Microtia in 55 Ears With Congenital External Ear Canal Anomalies
Relationship Between the Type of External Ear Canal Anomaly and Grade of Microtia in 55 Ears With Congenital External Ear Canal Anomalies
Table 3.  
Presence of the Manubrium in Relation to the Classification of External Auditory Canal Anomalies
Presence of the Manubrium in Relation to the Classification of External Auditory Canal Anomalies
1.
Jahrsdoerfer  RAYeakley  JWAguilar  EA  et al Grading system for the selection of patients with congenital aural atresia. Am J Otol.1992;13:6-12.
PubMed
2.
Lambert  PR Congenital aural atresia: stability of surgical results. Laryngoscope.1998;108:1801-1805.
PubMed
3.
Schuknecht  HF Congenital aural atresia. Laryngoscope.1989;99:908-917.
PubMed
4.
Mehra  YNDubey  SPMann  SBSuri  S Correlation between high-resolution computed tomography and surgical findings in congenital aural atresia. Arch Otolaryngol Head Neck Surg.1988;114:137-141.
PubMed
5.
Mayer  TEBrueckmann  HSiegert  R  et al High-resolution CT of the temporal bone in dysplasia of the auricle and external auditory canal. AJNR Am J Neuroradiol.1997;18:53-65.
PubMed
6.
Granstrom  GBergstrom  KTjellstrom  A The bone-anchored hearing aid and bone-anchored epithesis for congenital ear malformations. Otolaryngol Head Neck Surg.1993;109:46-53.
PubMed
7.
Farrior  J Surgical management of congenital conductive deafness. South Med J.1987;80:450-453.
PubMed
8.
Takegoshi  HKaga  KKikuchi  SIto  K Facial canal anatomy in patients with microtia: evaluation of the temporal bones with thin-section CT. Radiology.2002;225:852-858.
PubMed
9.
Takegoshi  HKaga  KKikuchi  SIto  K Mandibulofacial dysostosis: CT evaluation of the temporal bones for surgical risk assessment in patients of bilateral aural atresia. Int J Pediatr Otorhinolaryngol.2000;54:33-40.
PubMed
10.
Tomoda  KShea  JJShenefelt  REWilroy  RS Temporal bone findings in trisomy 13 with cyclopia. Arch Otolaryngol.1983;109:553-558.
PubMed
11.
Sando  ILeiberman  ABergstrom  L  et al Temporal bone histopathological findings in trisomy 13 syndrome. Ann Otol Rhinol Laryngol.1975;84:1-20.
PubMed
12.
Kountakis  SEHelidonis  EJahrsdoerfer  RA Microtia grade as an indicator of middle ear development in aural atresia. Arch Otolaryngol Head Neck Surg.1995;121:885-886.
PubMed
13.
Mallo  M Formation of the middle ear: recent progress on the developmental and molecular mechanisms. Dev Biol.2001;231:410-419.
PubMed
14.
Mallo  M Retinoic acid disturbs mouse middle ear development in a stage-dependent fashion. Dev Biol.1997;184:175-186.
PubMed
15.
Mallo  MGridley  T Development of the mammalian ear: coordinate regulation of formation of the tympanic ring and the external acoustic meatus. Development.1996;122:173-179.
PubMed
16.
Mallo  MSchrewe  HMartin  JF  et al Assembling a functional tympanic membrane: signals from the external acoustic meatus coordinate development of the malleal manubrium. Development.2000;127:4127-4136.
PubMed
17.
Martin  JFBradley  AOlson  EN The paired-like homeobox gene MHox is required for early events of skeletogenesis in multiple lineages. Genes Dev.1995;9:1237-1249.
PubMed
18.
Rivera-Perez  JAMallo  MGendron-Maguire  M  et al Goosecoid is not an essential component of the mouse gastrula organizer but is required for craniofacial and rib development. Development.1995;121:3005-3012.
PubMed
19.
Yamada  GMansouri  ATorres  M  et al Targeted mutation of the murine goosecoid gene results in craniofacial defects and neonatal death. Development.1995;121:2917-2922.
PubMed
20.
Marx  H Die Missbildungen des Ohres.  In: Henke  F, Lubarsh  O, eds.Handbuch der Spez Path Anat Hist. Berlin, Germany: Springer; 1926:620-625.
21.
Lambert  PRDonson  EE Congenital malformations of the external auditory canal. Otolaryngol Clin North Am.1996;29:741-760.
PubMed
22.
Donaldson  JADuckert  LGLambert  PM  et al Surgical Anatomy of the Temporal Bone.  New York, NY: Raven Press; 1992:1-139.
Original Article
August 2004

The Role of the External Auditory Canal in the Development of the Malleal Manubrium in Humans

Author Affiliations

From the Department of Otolaryngology, Faculty of Medicine, University of Tokyo, Tokyo, Japan. The authors have no relevant financial interest in this article.

Arch Otolaryngol Head Neck Surg. 2004;130(8):913-916. doi:10.1001/archotol.130.8.913
Abstract

Objective  To determine if the external auditory canal (EAC) plays a role in the induction and proper positioning of the malleal manubrium in humans.

Study Design  Retrospective study between 1994 and 2002.

Setting  Academic, tertiary care referral medical center.

Patients  Fifty-five ears of 50 patients with congenital atresia (n = 47) or stenosis (n = 8) of the EAC, for which meatoplasty was performed at the University hospital between 1994 and 2002.

Main Outcome Measures  The presence of the manubrium was examined during surgery, and the corre-lation between the presence of the manubrium and the grade of the microtia was evaluated.

Results  The manubrium was identified in all ears with EAC stenosis, whereas it was absent in all ears with EAC atresia. No correlation was observed between manubrium formation and auricular deformity.

Conclusions  Our results demonstrated a close relationship between the formation of the EAC and that of the malleal manubrium in humans. This is consistent with the recent findings in knockout mice. This information is useful for surgical intervention in cases of congenital EAC anomalies.

Congenital anomaly of the external auditory canal (EAC) is a relatively rare clinical entity and consists of a series of malformations of the auricle and EAC, the latter varying from slight narrowing to complete absence of the EAC.15 The incidence ranges from 1 in 10 0006 to 1 in 15 0007 births. A combination of reconstruction of the EAC and auricle is usually performed to achieve improvement in hearing and cosmetic appearance. The reconstruction of the anomalous EAC is one of the most challenging procedures in otology because it is often accompanied by middle ear anomalies, such as facial nerve aberration, deformity of the ossicles, defect of the oval window, and lack of mastoid pneumatization.15,8,9 These malformations are considered to result from developmental arrest between 6 and 10 weeks of fetal life.10,11 Knowledge of the development of middle ear elements is indispensable to safely and successfully complete surgery for congenital EAC anomalies. The patterns of formation of the middle ear elements and their mutual interaction, however, have not been fully explored in humans.

Preoperative evaluation with high-resolution computed tomography (HRCT) of the temporal bone is essential for surgical planning because it provides important information on the type and severity of anomalies of the EAC and middle ear elements, including the ossicles. The development of the middle ear has been evaluated by a grading system based on HRCT of the temporal bone.1 It has been reported that the severity of EAC and middle ear anomalies correlate with the surgical outcome.12

Recent molecular and genetic analyses using knockout mice enhance our understanding of ear development and the pattern of formation of middle ear elements.1316 For example, disappearance of the tympanic ring due to retinoic acid treatment and duplication of the ring in Hoxa-2 null mutant embryos resulted in alterations in EAC formation.15 In addition, Prx1 and Goosecoid (Gsc) genes are known to be essential for middle ear and EAC development, and target mutation of these genes results in the lack of tympanic ring and EAC and the hypomorphism of the manubrium.1719 These findings suggest that the formation of the EAC may depend on the formation of tympanic ring. Moreover, it has been reported that the presence of EAC plays an essential role in the induction and proper positioning of the malleal manubrium,13,16 which originates from the mesenchyme of the proximal area of the first branchial arch and provides the connection between the tympanic membrane and middle ear through skeletogenesis of the mesenchyme.13 These results obtained from genetically modified mice suggest a close correlation between the formation of the manubrium and the EAC. However, such a correlation has not been well documented in humans.

The purpose of the present study was to evaluate the relationship between the presence of the manubrium and the appearance of the EAC in humans by comparing them in ears with atresia or stenosis of the EAC.

METHODS

Between August 1992 and October 2002, reconstruction of the EAC was performed in 66 ears in 58 patients with EAC anomalies who had no known genetic abnormality. Eleven ears, in which the mesotympanum was not explored, were excluded. Thus, 55 ears of 50 patients (42 male and 8 female patients; mean age, 13.7 years [range, 6-34 years]) were included in the study. Eighteen patients had bilateral EAC anomalies, and 32 patients a unilateral anomaly (16 right-sided and 16 left-sided). Five patients underwent bilateral canaloplasties, and 45 patients underwent unilateral canaloplasty. Schuknecht3 established a classification (types A-D) of the atresia based on HRCT and surgical findings. In that classification, the EAC anomaly is limited in type A to the fibrocartilaginous part; the EAC is stenotic, and cholesteatoma sometimes develops in the EAC. In type B, narrowing and in some cases tortuosities of both the fibrocartilaginous and bony parts of the EAC are found. Type C has a totally atretic EAC with well-developed pneumatization of the tympanic cavity. Type D has poor pneumatization of the temporal bone with severe anomaly of the middle ear structures. We included types A and B in the stenosis group and types C and D in the atretic group.

The degree of microtia was classified into grades I to III according to the classification of Marx.20 Grade I microtia shows a mild deformity, with the auricle being slightly smaller than normal and each part being clearly distinguished. In grade II microtia, the size of the EAC is one half to two thirds of the normal size and its structure is partially retained. In grade III microtia, the auricle is severely malformed and usually exhibits a peanut shape.

The appearance of the ossicles was evaluated during surgery. We focused on 3 anatomical structures of the malleus. We evaluated the fusion of the malleus head with the incus body, presence of the neck and the lateral process of the malleus, and extension of the vertical process (ie, manubrium) below the lateral process. The surgical findings and the grades of microtia were compared between atresia and stenosis groups.

RESULTS

The number of ears in each of 4 atresia types (A-D) is given in Table 1. The stenosis group consisted of 8 ears of type B, whereas the atresia group consisted of 34 ears of type C and 13 ears of type D. The side of involvement was not associated with the type of EAC anomalies. The severity of microtia in relation to the degree of EAC stenosis is given in Table 2. Fifteen ears were assigned as grade I microtia, 9 ears as grade II, and 31 ears as grade III. Microtia was classified as grade I in 5 of 8 ears of type B, whereas microtia grade III was found in 11 of 13 ears of type D. Type C ears showed all grades of microtia with no prevalence. In general, the formation of the auricle was more severely affected in the atresia group compared with the stenosis group.

The relationship of the presence or absence of the manubrium and atresia or stenosis of the EAC is given in Table 3. The presence of manubrium was confirmed in all 8 ears of the stenosis group; however, the manubrium was shorter and angled toward the promontory in 5 of the ears. In the atresia group, the manubrium was absent in all ears. The head of the malleus and the body of the incus were commonly fused in this group. Figure 1 shows the HRCT and surgical findings of representative cases from each group.

COMMENT

Congenital anomalies of the EAC are often associated with absence or deformity of the manubrium or its angulation toward the promontory.15 Furthermore, the head of the malleus and the body of the incus are sometimes fused.15,9 The relationship between the pattern of the ossicles and the EAC condition, however, is not well understood. The present study clearly demonstrated a close relationship between the formation of the EAC and that of the malleal manubrium.

Schuknecht3 reported that in type C anomaly, the manubrium was "usually" absent, and when present, it was deformed and angled toward promontory. However, in that study, there was no reference to the correlation between the condition of the manubrium and ECA appearance. In addition, the relationship between the grade of the microtia and the presence of the manubrium was not clearly delineated. The present study demonstrated that the presence of the manubrium was dependent on the formation of the EAC but not on the severity of the microtia.

The EAC develops from the first branchial groove between the mandibular and hyoid arches of the dorsal and ventral portions.21,22In humans, at 4 to 5 weeks of gestation, a solid core of epithelial cells, derived from the ectoderm of the first groove, comes into contact with the endoderm of the first pharyngeal pouch, in the area of the tympanic ring.21,22 Then, the mesoderm grows between the ectoderm and the endoderm, and the contact is disrupted. By the eighth week of gestation, the primary meatus is formed like a funnel-shaped tube because of the deepening of the first branchial cleft toward the tympanic cavity.21,22 The primary meatus corresponds to the lateral third of the EAC, which is later surrounded by cartilage that forms from the surrounding mesoderm.21,22 During the ninth week of gestation, the ectoderm of the first branchial groove thickens and grows medially toward the tympanic cavity.21,22 During the 21st week of fetal life, resorption of the cord epithelial cells begins to occur, leading to the formation of a canal.21,22 By the 28th week, the deepest cells of the ectoderm plug remain, forming the superficial layer of the tympanic membrane.21,22 The medial two thirds of the EAC is derived from the new ectodermal tube and becomes the bony portion of the canal.21,22 If this canalization process is arrested prematurely, it is possible for a more normally developed tympanic membrane and bony ear canal to exist in association with an atretic or stenotic membranous canal.21,22

There is a close relation between the development of the tympanic ring and the formation of the manubrium.13 The manubrium of the malleus is inserted in the tympanic membrane. This process is essential for transferring vibrations in the membrane to ossicle chain. The anatomical structure of the insertion of the manubrium between 2 epithelia is due to the development of the EAC, tympanic membrane, and the middle ear cavity.13 In particular, the tympanic ring plays a central role in the anatomical structure.13 Moreover, the development of the tympanic ring is induced by the formation of the EAC, and the development of the manubrium is dependent on the formation of the EAC. These correlations may explain why the manubrium was absent in the atresia group but present, albeit short and deformed, in the stenosis group.

In conclusion, we have demonstrated in the present study that the formation of the manubrium was closely associated with the appearance of the EAC, suggesting that the EAC also plays an essential role in the induction and proper location of the malleal manubrium in humans.

Back to top
Article Information

Correspondence: Shin-ichi Ishimoto, MD, Department of Otolaryngology, Faculty of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan (shinchan-tky@umin.ac.jp).

Submitted for publication September 9, 2003; final revision received December 15, 2003; accepted December 18, 2003.

References
1.
Jahrsdoerfer  RAYeakley  JWAguilar  EA  et al Grading system for the selection of patients with congenital aural atresia. Am J Otol.1992;13:6-12.
PubMed
2.
Lambert  PR Congenital aural atresia: stability of surgical results. Laryngoscope.1998;108:1801-1805.
PubMed
3.
Schuknecht  HF Congenital aural atresia. Laryngoscope.1989;99:908-917.
PubMed
4.
Mehra  YNDubey  SPMann  SBSuri  S Correlation between high-resolution computed tomography and surgical findings in congenital aural atresia. Arch Otolaryngol Head Neck Surg.1988;114:137-141.
PubMed
5.
Mayer  TEBrueckmann  HSiegert  R  et al High-resolution CT of the temporal bone in dysplasia of the auricle and external auditory canal. AJNR Am J Neuroradiol.1997;18:53-65.
PubMed
6.
Granstrom  GBergstrom  KTjellstrom  A The bone-anchored hearing aid and bone-anchored epithesis for congenital ear malformations. Otolaryngol Head Neck Surg.1993;109:46-53.
PubMed
7.
Farrior  J Surgical management of congenital conductive deafness. South Med J.1987;80:450-453.
PubMed
8.
Takegoshi  HKaga  KKikuchi  SIto  K Facial canal anatomy in patients with microtia: evaluation of the temporal bones with thin-section CT. Radiology.2002;225:852-858.
PubMed
9.
Takegoshi  HKaga  KKikuchi  SIto  K Mandibulofacial dysostosis: CT evaluation of the temporal bones for surgical risk assessment in patients of bilateral aural atresia. Int J Pediatr Otorhinolaryngol.2000;54:33-40.
PubMed
10.
Tomoda  KShea  JJShenefelt  REWilroy  RS Temporal bone findings in trisomy 13 with cyclopia. Arch Otolaryngol.1983;109:553-558.
PubMed
11.
Sando  ILeiberman  ABergstrom  L  et al Temporal bone histopathological findings in trisomy 13 syndrome. Ann Otol Rhinol Laryngol.1975;84:1-20.
PubMed
12.
Kountakis  SEHelidonis  EJahrsdoerfer  RA Microtia grade as an indicator of middle ear development in aural atresia. Arch Otolaryngol Head Neck Surg.1995;121:885-886.
PubMed
13.
Mallo  M Formation of the middle ear: recent progress on the developmental and molecular mechanisms. Dev Biol.2001;231:410-419.
PubMed
14.
Mallo  M Retinoic acid disturbs mouse middle ear development in a stage-dependent fashion. Dev Biol.1997;184:175-186.
PubMed
15.
Mallo  MGridley  T Development of the mammalian ear: coordinate regulation of formation of the tympanic ring and the external acoustic meatus. Development.1996;122:173-179.
PubMed
16.
Mallo  MSchrewe  HMartin  JF  et al Assembling a functional tympanic membrane: signals from the external acoustic meatus coordinate development of the malleal manubrium. Development.2000;127:4127-4136.
PubMed
17.
Martin  JFBradley  AOlson  EN The paired-like homeobox gene MHox is required for early events of skeletogenesis in multiple lineages. Genes Dev.1995;9:1237-1249.
PubMed
18.
Rivera-Perez  JAMallo  MGendron-Maguire  M  et al Goosecoid is not an essential component of the mouse gastrula organizer but is required for craniofacial and rib development. Development.1995;121:3005-3012.
PubMed
19.
Yamada  GMansouri  ATorres  M  et al Targeted mutation of the murine goosecoid gene results in craniofacial defects and neonatal death. Development.1995;121:2917-2922.
PubMed
20.
Marx  H Die Missbildungen des Ohres.  In: Henke  F, Lubarsh  O, eds.Handbuch der Spez Path Anat Hist. Berlin, Germany: Springer; 1926:620-625.
21.
Lambert  PRDonson  EE Congenital malformations of the external auditory canal. Otolaryngol Clin North Am.1996;29:741-760.
PubMed
22.
Donaldson  JADuckert  LGLambert  PM  et al Surgical Anatomy of the Temporal Bone.  New York, NY: Raven Press; 1992:1-139.
×