Embryology and anatomy of the ear

Embryology and anatomy of the ear

Author’s Accepted Manuscript Embryology and anatomy of the ear Lauren B. Moneta, Lourdes Quintanilla-Dieck www.techgiendoscopy.com PII: DOI: Referen...

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Author’s Accepted Manuscript Embryology and anatomy of the ear Lauren B. Moneta, Lourdes Quintanilla-Dieck

www.techgiendoscopy.com

PII: DOI: Reference:

S1043-1810(17)30039-8 http://dx.doi.org/10.1016/j.otot.2017.03.011 YOTOT761

To appear in: Operative Techniques in Otolaryngology - Head and Neck Surgery Cite this article as: Lauren B. Moneta and Lourdes Quintanilla-Dieck, Embryology and anatomy of the ear, Operative Techniques in Otolaryngology Head and Neck Surgery, http://dx.doi.org/10.1016/j.otot.2017.03.011 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Embryology and Anatomy of the Ear Lauren B. Moneta, MD and Lourdes Quintanilla-Dieck, MD

Positions: Lauren B. Moneta, MD Resident Physician Department of Otolaryngology Head & Neck Surgery Oregon Health & Science University

Lourdes Quintanilla-Dieck, MD Assistant Professor Department of Otolaryngology Head & Neck Surgery Oregon Health & Science University Contact address: PV-01, 3181 Sam Jackson Park Road Portland, Oregon 97232

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Phone: 503-494-1446 Fax: 503-494-4631 Email: [email protected]

Disclosures: The authors report no proprietary or commercial interest in any concept discussed in this article. Illustrator credit: All art work is original and created by Lauren B. Moneta, MD.

Abstract External ear anomalies are common and range from mild asymmetries to severe deformity or complete lack of external ear development. An in depth knowledge of the developmental stages and embryology allows for an understanding of patterns of ear malformation. Here we review the embryology of the ear as well as the anatomy of a normally formed ear as a preface for discussing reconstruction in future chapters of this issue. Key Words: ear embryology, ear anatomy

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Introduction Ear malformations are common and range from minor abnormalities to complete anotia (lack of an ear). Understanding the key steps in the embryologic development of the external ear is therefore critical to the understanding of various ear deformities. Although we will briefly discuss embryology of the ear canal, the focus of this discussion is on external ear development. Embryology of the External Ear In the development of the human ear, the branchial arches play a crucial role. They are separated by pouches composed of endoderm on the internal aspect and by clefts composed of ectoderm on the external side. The central mesoderm contains the muscle, cartilage, vessels and nerves that will ultimately supply and establish the surrounding anatomic structures (Figure 1). Molecular signaling from the ectoderm results in invasion of mesenchyme and gradual obliteration of the clefts and pouches. The importance of this mesenchymal invasion is highlighted by the fact that failure of this critical step leads to remnants of the brachial arches and clefts, resulting in various auricular anomalies. Type I branchial cleft cysts represent a persistence of the first branchial cleft1. Additionally, some suggest that when there is an anomaly in the molecular signaling between the ectoderm and mesenchyme it can lead to failure of chondrogenesis. This breakdown of signaling can result in different degrees of

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anomalies, from absence of specific auricle components to microtia or even anotia if there is complete chondrogenesis failure2,3. Development of the human ear begins with appearance of the otic placode and vestibulocochlear ganglia at three weeks of gestation. The external auditory canal (EAC) begins to develop from the first branchial cleft at four weeks. A pit is then formed by ectodermal proliferation. By 28 weeks an epithelial core has canalized from medial to lateral resulting in the fully patent EAC. When the external auditory meatus fails to canalize, it can result in membranous or bony stenosis or atresia4. Development of the auricle begins at five weeks gestation with development of the auricular hillocks numbered from one through six, derived from the first (mandibular) and second (hyoid) branchial arches4. By the sixth week there are six mesenchymal thickenings at the dorsal margins of the first and second branchial arches5. The first and sixth hillocks become more distinct before the remainder of the hillocks but all are defined by the end of week six6. Fusion of the hillocks results in formation of the auricle. It has been proposed that failure of these hillocks to fuse results in the formation of preauricular pits or sinuses and cleft ear (Figure 2)7,8. An overview of embryonic ear development is highlighted in Table 1.

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The contributions of each hillock become less defined in the transitional zone between the mandibular and hyoid arches5. While it is mostly agreed upon that the hillocks can be followed through development to specific components of the auricle, this theory has been doubted by some who state the hillocks are transient, representing intense foci of mesenchymal proliferation which do not directly give way to specific auricle components2. Specifically there is controversy regarding the developmental origin of the ascending helix and crus helicis. Over time the exact contributions of the each hillock to the auricle have been modified, starting with His in 1885. Park proposed that the pinna may develop from hillocks one and six based on his surveillance of ear clefting deformities9. An additional contribution to the auricular primordium is the free ear fold which develops posterior to the second branchial arch and ultimately gives rise to part of the helix, scaphoid fossa and to the superior crus of the antihelix10. Table 2 summarizes the proposed contributions of each hillock to the final auricle while Figure 3 illustrates these contributions throughout embryonic development. Finally, movement of the auricle within the human embryo was described in detail by Streeter in 192210. During development, the external ear gradually moves laterally and dorsally and in the cranial direction relative to the eyes and mouth. Kagurasho et al determined that movement of the ear during development is based on changes in size and shape of the embryo also known as differential growth, rather than on migration from one area to another11.

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Anatomy The auricle plays a minor but important role in hearing. The auricle serves to help localize sound and the concha has a resonance of approximately 5 kHz4. As mentioned previously, during embryologic development the ear’s components are derived from the hillocks. The central mesenchyme is essential as it carries components leading to vascular, nerve and muscular supply for the ear. The vascular supply of the ear is composed of a complex network of interconnected vessels stemming mainly from the superficial temporal artery (STA) and the posterior auricular artery8 (Figure 4). There are variable branch patterns of upper, middle and lower terminal branches of the STA that contribute to the anterior blood supply. Further anterior arterial contributions come from the perforating branches of the posterior auricular artery. Venous drainage is variable but most often originates from venae comitantes that accompany one of the two main arteries. Skin over the anterior and posterior surfaces differs mostly in its mobility with the posterior skin being quite mobile and the anterior skin tightly adherent to the underlying cartilage. The postauricular region contains a layer of connective tissue carrying blood vessels and nerves that separates the skin from the perichondrium. This becomes relevant when pursuing reconstructive options as one must consider the fascial layer in addition to the cutaneous layer.

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Sensory innervation of the auricle is variable as was demonstrated by Peuker and Filler in 200212. The lobule, antitragus, scapha, superior and inferior crurae and posterior helix are almost uniformly innervated by the great auricular nerve (GAN). The GAN overlaps with the auriculotemporal nerve (ATN) in most cases to provide innervation to the tragus. The ATN is the predominant nerve supply for the anterior helix and the root of the helix. The auricular branch of the vagus nerve (ABVN) also provides innervation to the antihelix the majority of the time. However, the ABVN has accessory innervation roles in the superior and inferior crurae and contributes to innervation of the middle and lower one-third of the cranial (posterior) surface. The final contribution comes from the lesser occipital nerve (LON). The LON contributes to the innervation of the upper third and middle third of the cranial surface. Common innervation is illustrated in Figure 5. The topographic landmarks are important for creating the distinctive look of the human ear. Their names and relationships are important for describing anomalies and defects and must be considered during reconstruction. The most external portion of the auricle is the helix which can further be divided into four sections: the root, anterior helix, superior helix and posterior helix, depicted in Figure 6. At the inferior aspect of the helix is the lobule, the only part of the auricle that does not contain any cartilage but rather is made up of skin and fibrofatty tissue. Working from external to internal the next section of the auricle is the antihelix. The antihelix can be divided into three parts: the body, superior crus and inferior

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crus. Inferiorly the body blends with the antitragus which opposes the tragus and the root of the helix on the anterior portion of the auricle (Figure 6). The cartilaginous components of the anterior auricle consist of named depressions or fossae outlined by prominences. The scaphoid and triangular fossae are posterior and anterior to the superior crus of the antihelix, respectively. The middle fossa is the concha which is divided into the concha cymba, superior to the root of the helix, and the concha cavum inferiorly. More inferiorly the intertragal notch is posterior to the tragus and anterior to the antitragus (Figure 6). On the posterior surface of the auricle are the scaphoid, triangular and conchal eminences, whose names parallel the corresponding fossa on the anterior surface of the auricle. The superior and inferior crura on the anterior surface are complemented by the superior and inferior grooves on the posterior surface. The ponticulus, a vertical ridge which crosses the conchal eminence, can also be seen in about 66% of ears13. The muscles of the auricle are divided into intrinsic and extrinsic (Figure 7). The three extrinsic muscles include the superior, anterior and posterior auricularis muscles. The six intrinsic muscles are considered vestigial but may play a role in modifying the shape of the auricle. The intrinsic muscles include the helicis major and minor, tragicus, antitragicus, traversus auriculae and obliquus

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auriculae. Details of the origins, insertions and innervations of the auricular muscles can be found in Table 3. By three years of age, 85% of ear growth is complete and adult size is reached by six years of age14. Overall the average height of the adult auricle is approximately 58 mm for females and 62 mm for males. Projection of the auricle is defined as the distance from the posterior region of the middle helix to the mastoid skin and the normal range is 15 to 21 mm in both males and females 14. The scaphoconchal angle should be approximately 90˚ and the normal range of the cephaloauricular angle is defined as anywhere from 20-35˚ 14,15 . Conclusions The ear develops in a predictable manner, with various alterations in development resulting in predictable deformities when the process is interrupted. Knowledge of auricular development as well as normal external anatomy allows for precise evaluation of the ear and assists in selecting appropriate reconstructive techniques to optimize the complex three dimensional anatomical outcomes that will be discussed in the following articles.

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References: 1. Waldhausen JHT. Branchial cleft and arch anomalies in children. Semin Pediatr Surg 2006; 15(2): 64-69. 2. Porter CJW, Tan ST. Congenital auricular anomalies: Topographic anatomy, embryology, classification and treatment strategies. Plast Reconstr Surg 2005; 115(5): 1701-1712. 3. Cousley RR, Wilson DJ. Hemifacial macrosomia: Developmental consequence of perturbation of the auriculofacial cartilage model? Am J Med Genet 1992; 42(4): 461-466. 4. Wareing MJ, Lalwani AK, Anwar AA, Jackler RK. Development of the ear. Philadelphia (PA): Wolters Kluwer Health/Lippincott Williams & Wilkins; 2014. (Johnson JT, Rosen CA, Bailey BJ, editors. Bailey’s Head and Neck Surgery-Otolaryngology.) 5. Park C and Roh TS. Congenital upper auricular detachment. Plast Reconstr Surg 1999; 104: 488-490. 6. Wood-Jones, F and Wen IC. The development of the external ear. J Anat 1933; 68: 525-533. 7. Emery PJ, Salaman NY. Congenital preauricular sinus: a study of 31 cases seen over a 10-year period. Int J Pediatr Otorhinolaryngol 1981; 3: 205218.

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8. Park C, Roh TS. Anatomy and embryology of the external ear and their clinical correlation. Clin Plast Surg 2002; 29: 155-174. 9. Park C. Lower auricular malformations: Their representation, correction and embryologic correlation. Plast Reconstr Surg 1999; 104: 29-40. 10. Streeter, GL. Development of the auricle in the human embryo. Carnegie Contrib Embryol 1922; 14: 111-148. 11. Kagurasho M, Shigehito Y, Uwabe C, Kose K, Takakuwa T. Movement of the external ear in the human embryo. Head Face Med 2012; 8: 1-9. 12. Peuker ET, Filler TJ. The nerve supply of the human auricle. Clin Anat 2002;15: 35-37. 13. Holt JJ. The ponticulus: an anatomic study. Otol Neurotol 2005; 26(6): 1122-1124. 14. da Silva Freitas R, Sanchez MER, Manzotti MS, Baras F, Ono MCC, de Olivera e Cruz GA. Comparing cephaloauricular and scaphaconchal angles in prominent ear patients and control subjects. Aesthetic Plast Surg 2008; 32(4): 620-623. 15. Farkas LG. Vertical and horizontal proportion of the face in young adult North American Caucasions: revisions of neo-classical canons. Plast Reconstr Surg 1975;27:446-453.

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Table 1. Summary of fetal development of the external ear. Week of

Embryonic

Possible

Development

Event

Malformation(s)

3

Development of otic placode Vestibulocochlear ganglia appear

4

Beginning of EAC development

5

First sign of auricular hillocks

6

Auricular hillocks fully distinct

6-8

Hillocks fuse to form auricular

Failure of fusion:

structure

preauricular sinuses and pits; cleft ear deformities

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9-18

Auricular structure evident

Signaling failure results

Epithelial strand that will become

in arrest of development:

EAC apparent

possible microtia or

Migration of auricle components

anotia

and continued development 18

Auricle has final form (not size)

20

Beginning of disintegration of

Failure of disintegration:

external auditory meatal plug

EAC stenosis or atresia

28

EAC fully patent

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Table 2: Contributions of the arches and hillocks to the human auricle. Branchial Hillock

Ear

Arch

Number Component

Arch 1

1

Tragus

Arch 1

2

Crus helicis

Arch 1

3

Ascending helix

Arch 2

4

Horizontal helix, upper portion of scapha, antihelix

Arch 2

5

Descending helix, middle scapha, antihelix

Arch 2

6

Antitragus, inferior helix

Table 3. Muscles of the auricle. Muscle

Origin

Auriculari

Galea

s anterior

aponeuros

Insertio

Innervatio

n

n

Helix

CN VII

Action

Extrinsic/Intrins ic

Pulls ear

Extrinsic

forward

is Auriculari

Mastoid

Posterior

CN VII

13

Pulls ear

Extrinsic

s posterior

process

root of

backwar

the ear

d

Auriculari

Galea

Upper

CN VII

Pulls ear

s superior

aponeuros

posterior

upward

is

ear

and

Extrinsic

backwar d Helicis

Root helix

Anterior

CN VII

None

Intrinsic

CN VII

May

Intrinsic

border

major

helix Helicis

Base root

Anterior

minor

of the

helix

contribut

helix

e to shape of anterior margin of ear

Antitragic

Outer

Tail of

CN VII

us

antitragus

helix and

modify

antihelix

shape

14

May

Intrinsic

auricle Tragicus

Base

Apex

tragus

tragus

CN VII

May

Intrinsic

increase opening of EAC

Obliquus

Conchal

Triangul

auriculae

Eminence

ar

CN VII

Flattens

Intrinsic

Auricle

Eminenc e Transvers

Conchal

Scapha

us

eminence

eminence

CN VII

Flattens auricle

auriculae

15

Intrinsic

16

17

18

19

20

21

22