AJR 2002; 178:1523-1530
© American Roentgen Ray Society
Hemifacial Microsomia in Pediatric Patients: Asymmetric Abnormal Development of the First and Second Branchial Arches
Raymond W. Sze1,
Angelisa M. Paladin1,
Samson Lee2 and
Michael L. Cunningham3
1 Department of Radiology, Children's Hospital & Regional Medical Center,
4800 Sand Point Way N.E., CH-69, Seattle, WA 98105.
2 Department of Otolaryngology, University of Washington, 1959 N.E. Pacific St.,
Seattle, WA 98195.
3 Children's Craniofacial Center, Children's Hospital & Regional Medical
Center, Seattle, WA 98105.
Received July 3, 2001;
accepted after revision December 7, 2001.
R. W. Sze is a 2001-2002 American Roentgen Ray Society
Scholar.
Presented at the annual meeting of the American Roentgen Ray Society,
Seattle, April—May 2001.
Address correspondence to R. W. Sze.
Introduction
Hemifacial microsomia is the second most common developmental craniofacial
anomaly after cleft lip and palate and affects one of every 5600 live births
[1]. More than 15 terms,
including Goldenhar's syndrome and oculoauriculovertebral dysplasia, have been
applied to this disease, with each term representing the perspectives of
different specialists. Diagnostic imaging is important in the presurgical
evaluation of patients with this anomaly; however, the broad spectrum of
abnormalities encountered in patients with hemifacial microsomia can be
confusing.
Hemifacial microsomia results from the abnormal development of the first
and second branchial arches and the first branchial membrane. In this
pictorial essay, the embryology of the first and second branchial arches and
the first branchial membrane are reviewed and applied to detecting the facial
musculoskeletal and ear abnormalities seen on CT studies of patients with
hemifacial microsomia.
Facial Musculoskeletal Structures and Ossicles
Branchial Arch Development
The branchial arches initially consist of mesenchyme derived from lateral
mesoderm. Beginning in the fourth week of gestation, the branchial arches
swell into discrete structures as neural crest cells migrate into the arches
of the future head and neck [2]
(Fig.
1A,1B).
Neural crest cells differentiate in the lateral lips of the neural folds and
detach during neurulation. Neural crest cells then migrate throughout the
head, neck, and body to form diverse structures including the cardiac
conotruncal septum, adrenal medulla, and melanocytes. Each branchial arch
contains cartilaginous precursors and muscle anlage derived from the neural
crest, an arch artery, and a cranial nerve (Fig.
2A,2B).
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Fig. 1A. —Drawings illustrate migration of neural crest cells and
development of branchial arches. Neural crest cells (NC) form as neural plate
folds and meets in midline to form neural tube (NT). These cells then migrate
throughout body to form diverse structures of head, neck, and body.
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Fig. 1B. —Drawings illustrate migration of neural crest cells and
development of branchial arches. Branchial arches develop in craniocaudal
sequence. First branchial arch (I) begins to form at approximately day 22 of
gestation; second (II) and third (III) arches, at day 24 of gestation; and
fourth (IV) and sixth (VI) arches, at day 29 of gestation.
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Fig. 2A. —Drawings illustrate branchial arch and membrane anatomy at
approximately 5 weeks' gestation. First (I), second (II), third (III), fourth
(IV), and sixth (VI) branchial arches are shown. Plane of section through
branchial arches corresponds to interrupted line in
Figure 1B. Area outlined by
rectangle illustrates cross-sectional anatomy of one branchial arch.
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Fig. 2B. —Drawings illustrate branchial arch and membrane anatomy at
approximately 5 weeks' gestation. Each arch contains arch-specific cartilage
(C), muscle anlage (M), artery (A), and cranial nerve (CN). Inner branchial
pouch (FBP) is lined by endoderm (EN), and outer branchial cleft (groove)
(FBC) is lined by ectoderm (EC). Branchial membrane (FBM) consists of
endodermal cells of branchial pouch, ectodermal cells of branchial cleft, and
intervening mesoderm.
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First Branchial Arch
The mandible, maxilla, zygomatic temporal bone, and squamous temporal bone
form from the direct ossification of the first-arch dermal mesenchyme
[2]
(Fig. 3A) Asymmetric
development of the mandible is a diagnostic hallmark of hemifacial microsomia,
and accurate assessment of the mandible is essential for presurgical planning
[3] (Fig.
4A,4B).
A common classification system for the mandible uses 1 for a small but
normally shaped mandible; 2 for a small and abnormally shaped mandible, with
2A designating that the condyle is in the normal position and 2B that the
condyle is displaced; and 3 for aplasia of the ramus and condyle
[4].
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Fig. 3A. —Drawings show first branchial arch derivatives. Arch dermal
mesenchyme forms mandible, maxilla, zygomatic temporal bone, and squamous
temporal bone (ST) through direct ossification. First-arch cartilage
derivatives include malleus (M); incus (I); alisphenoid (greater wing of
sphenoid); and small fibrous core in mandible, which is called Meckel's
cartilage (MC).
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Fig. 4A. —Facial bones in 4-year-old girl with left hemifacial
microsomia. Three-dimensional CT reconstruction shows hypoplastic, malformed
left mandibular body, ramus, and condyle (arrow) that does articulate
with glenoid fossa (type 2A mandible). Zygomatic arch (arrowhead) is
incomplete, and maxilla and squamous temporal bone are small. Note bony
atresia of external auditory canal.
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Fig. 4B. —Facial bones in 4-year-old girl with left hemifacial
microsomia. Three-dimensional CT reconstruction of contralateral side with
normal appearance of mandible, maxilla, zygomatic arch, squamous temporal
bone, external auditory canal, and temporomandibular joint
(arrow).
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Most embryology textbooks describe the malleus and incus as being
pre-formed in arch cartilage from the first branchial arch
[2]
(Fig. 3A). Other authors have
proposed a more complex origin: the first arch contributes to the malleus head
and neck and the incus body and short process, and the manubrium of the
malleus and the long process of the incus are then derived from the second
branchial arch cartilage [5].
Common abnormalities seen in patients with hemifacial microsomia include
malformation and fusion of the malleus and incus and lateral displacement of
the malleus and incus against the lateral wall of the tympanic cavity
[4] (Fig.
5A,5B,5C,5D).
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Fig. 5A. —Temporal bone in 4-year-old boy with left hemifacial
microsomia. Coronal CT scan obtained through right temporal bone shows normal
malleus (arrow), tympanic cavity, external auditory canal, and
pinna.
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Fig. 5B. —Temporal bone in 4-year-old boy with left hemifacial
microsomia. Coronal CT scan obtained through left temporal bone shows fused,
malformed malleus and incus (arrow), which are displaced and fused to
lateral wall of tympanic cavity. Note bony and soft-tissue atresia of external
auditory canal. Pinna is small and malformed.
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Fig. 5C. —Temporal bone in 4-year-old boy with left hemifacial
microsomia. Axial CT scan obtained through right temporal bone shows normal
malleoincudal articulation (straight arrow) and tensor tympani muscle
(wavy arrow). Inner ear structures are normal.
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Fig. 5D. —Temporal bone in 4-year-old boy with left hemifacial
microsomia. Axial CT scan obtained through left temporal bone shows fusion of
malleus and incus (arrowhead), small tensor tympani muscle
(arrow), and malformed pinna. Inner ear structures are normal.
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The muscles of mastication are derived from the muscle anlage of the first
branchial arch (Fig. 3B).
Hypoplasia of these muscles leads to cosmetic and functional asymmetry of the
facial soft tissues. Although development of the masticatory muscles is
intimately associated with the osseous muscle attachment sites, the morphology
of the bones does not allow prediction of the muscle mass, and the muscles
require independent evaluation
[6]. Imaging assessment yields
significantly more information about the status of these muscles than is
available through clinical examination (Fig.
6A,6B,6C).
The tensor tympani muscle, the anterior belly of the digastric muscle, the
mylohyoid muscle, and the tensor muscle of the velum palatinum are also
derived from the first arch, and asymmetric development of these structures
can be detected on imaging studies (Figs.
5C,
5D, and
7).
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Fig. 3B. —Drawings show first branchial arch derivatives. Muscle anlage
of first branchial arch gives rise to muscles required for
mastication—temporal (T), masseter (M), medial and lateral pterygoids
(P)—and to anterior belly of digastric muscle (ABD), tensor tympani
muscle (TT), mylohyoid muscle (MH), and tensor muscle of velum palatinum.
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Fig. 6A. —Muscles of mastication in 7-year-old girl with left
hemifacial microsomia. Axial CT scan shows normal right masseter muscle
(straight arrow) and medial pterygoid muscle (arrowhead)
compared with hypoplastic left medial pterygoid muscle (wavy arrow)
and essentially absent masseter muscle. Patient has complex segmentation
anomalies of cervical spine resulting in left convex scoliosis and eccentric
position of dens relative to anterior arch of C1. These vertebral anomalies,
which are traditionally associated with Goldenhar's syndrome, are now
generally considered part of spectrum of findings associated with hemifacial
microsomia.
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Fig. 6B. —Muscles of mastication in 7-year-old girl with left
hemifacial microsomia. CT scan shows normal right lateral pterygoid muscle
inserting along lateral surface of lateral pterygoid plate (straight
arrow). On left, small and poorly formed lateral pterygoid muscle
(arrowhead) can be identified by its insertion on hypoplastic lateral
pterygoid plate. Lateral pterygoid muscle is difficult to distinguish from
medial pterygoid muscle, which inserts into pterygoid fossa. Muscle lying
lateral to lateral pterygoid fossa is temporal muscle (wavy arrow),
which inserts inferiorly on dysplastic mandible.
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Fig. 6C. —Muscles of mastication in 7-year-old girl with left
hemifacial microsomia. Axial CT scan obtained through level of temporal fossae
shows normal temporal muscle on right (arrowhead) and hypoplasia of
contralateral temporal muscle on left (arrow). Left zygomatic arch is
incomplete. Note bony atresia of left external auditory canal.
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Fig. 7. —Anterior belly of digastric muscle in 4-year-old girl with
left hemifacial microsomia. Axial CT scan obtained through floor of mouth
shows normal right anterior belly of digastric muscle (arrowhead) and
atresia of left anterior digastric muscle. Rounded soft-tissue structure
adjacent to anterior digastric muscle is submandibular gland.
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Second Branchial Arch
The second branchial arch contributes little to facial development relative
to the first arch. Second arch cartilage derivatives include the stapes,
lesser horn and upper rim of the hyoid bone, styloid process, and stylohyoid
ligament [2] (Figs.
8A and
9). The muscle anlage of the
second branchial arch gives rise to the muscles of facial expression,
posterior belly of the digastric muscle, the stapedius muscle, and the
stylohyoid muscle [2] (Figs.
8B and
10A,10B,10C,10D).
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Fig. 8A. —Drawings show derivatives of second branchial arch. Cartilage
derivatives of second branchial arch include stapes (S), styloid process (SP),
stylohyoid ligament (SL), and lesser horns and upper rim of hyoid bone
(H).
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Fig. 9. —Hyoid bone in 11-year-old girl with left hemifacial
microsomia. Axial CT scan obtained through hyoid bone shows absence of left
lesser and greater horn of hyoid bone; greater horn is derived from third
branchial arch. Normal lesser horn (arrowhead) and greater horn
(arrow) are visible on right.
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Fig. 8B. —Drawings show derivatives of second branchial arch. Muscle
anlage of second branchial arch gives rise to muscles of facial expression
including orbicular muscle of mouth (OM) and of eye (OE), nasal muscle (N),
levator muscle of upper lip, greater and lesser zygomatic muscles, buccinator
muscle (B), auricular muscles (A), and occipitofrontal muscle (OF). Other
muscles that originate from second branchial arch are posterior belly of
digastric muscle (PBD), stapedius muscle (S), and stylohyoid muscle (SH).
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Fig. 10A. —Muscles of facial expression in 13-year-old girl with right
hemifacial microsomia. CT scan shows that left orbicular muscle of mouth has
normal bulk (arrow), whereas right is atretic.
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Fig. 10B. —Muscles of facial expression in 13-year-old girl with right
hemifacial microsomia. CT scan shows bulk of left levator muscle of upper lip
(straight arrow) and greater zygomatic muscle (arrowhead)
compared with atretic right side. Also note atretic right mandibular ramus
(wavy arrow).
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Fig. 10C. —Muscles of facial expression in 13-year-old girl with right
hemifacial microsomia. CT scan shows left orbicularis oculi muscle is normal
(arrow), but right orbicularis oculi muscle is barely visible. Note
bony atresia of right external auditory canal and malformed, small, and
flattened pinna (arrowhead).
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Fig. 10D. —Muscles of facial expression in 13-year-old girl with right
hemifacial microsomia. CT scan shows left frontalis muscle is thin soft-tissue
sheet that can be seen over the frontal bone (arrow). Atretic right
muscle can barely be detected. Note normal bulk of left temporal muscle in
temporal fossa (arrowhead) in contrast to atretic right temporal
muscle.
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External, Middle, and Inner Ear
Auricular Hillocks
The pinna develops from six hillocks of the first and second branchial
arches that arise on either side of the first branchial cleft
[2] (Fig.
11A,11B,11C).
The second arch contributes to the majority of the final pinna. Abnormal
development of the auricular hillocks leads to microtia or atresia of the
pinna and is proportional in severity to the severity of the abnormal external
auditory canal development [4]
(Figs.
5A,5B,5C,5D,
6A,6B,6C,
and
10A,10B,10C,10D).
Abnormal accessory hillocks become preauricular tags seen in some patients
with hemifacial microsomia.
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Fig. 11A. —Drawings illustrate development of pinna. Areas with black
dots = first branchial arch, areas with white dots = second branchial arch.
Pinna originally arises from six swellings, or auricular hillocks (AH), of
first (FBA) and second branchial arches (SBA), which flank first branchial
cleft (FBC).
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Fig. 11B. —Drawings illustrate development of pinna. Areas with black
dots = first branchial arch, areas with white dots = second branchial arch.
Auricular hillocks fuse and remodel to form structures of immature pinna.
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Fig. 11C. —Drawings illustrate development of pinna. Areas with black
dots = first branchial arch, areas with white dots = second branchial arch.
Pinna is fully formed and predominantly originates from second branchial
arch.
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First Branchial Cleft (Groove)
The external auditory canal begins as a deepening of the ectoderm-lined
first branchial cleft [2] (Fig.
11A,11B,11C).
The ectodermal lining cells of the developing external auditory meatus
proliferate to form a meatal plug that subsequently recanalizes. The failure
of cleft deepening or of recanalization of the meatal plug results in various
degrees of soft-tissue and bony external auditory canal atresia or stenosis
(Figs.
4A,4B,5A,5B,5C,5D,6A,6B,6C
and
10A,10B,10C,10D).
Cysts of the first branchial cleft and the branchial sinus result from buried
cell rests or unobliterated sinuses
[7] but are not associated with
hemifacial microsomia.
First Branchial Pouch
The tympanic cavity is formed by elongation of the endoderm-lined first
branchial pouch [2] (Fig.
12A,12B,12C).
This tubotympanic recess eventually cavitates around the mesoderm-embedded
ossicles (independently derived from the cartilage of the first and second
arches), leaving a layer of endoderm over the ossicles. The expanding tympanic
cavity remains connected to the pharynx via the narrow auditory tube and abuts
the forming tympanic membrane. The tympanic membrane consists of an inner
layer of endoderm, a middle layer of mesoderm, and an outer layer of ectoderm.
Patients with aural atresia who have a facial nerve course overlying the oval
window or a tympanic cavity measuring less than 3 mm from the medial
promontory of the cochlea to the lateral area of bony plate atresia are
considered unfavorable candidates for surgery
[8] (Fig.
13A,13B).
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Fig. 12A. —Drawings reveal development of external, middle, and inner
ear. Gray area = cartilage condensations of neural crest origin, areas with
horizontal lines = ectoderm, areas with diagonal lines = endoderm. First
branchial cleft (FBC) will become external auditory canal, first branchial
pouch (FBP) will become auditory canal (eustachian tube) and tympanic cavity,
and otic vesicle (OV) (ectodermal derivative) will give rise to membranous
labyrinth. Ossicles (OC) are formed from cartilage condensations of neural
crest origin. EA = endolymphatic appendage, AH = auricular hillocks.
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Fig. 12B. —Drawings reveal development of external, middle, and inner
ear. Gray area = cartilage condensations of neural crest origin, areas with
horizontal lines = ectoderm, areas with diagonal lines = endoderm.
Medial-developing external auditory canal becomes filled with meatal plug (MP)
consisting of proliferating ectodermal cells that subsequently recanalize.
Tubotympanic recess (TR) has deepened to form tympanic cavity (TC). Otic
vesicle forms endolymphatic duct and sac (ES), early semicircular canals (SC),
and cochlear diverticulum (CD). Membranous labyrinth induces surrounding
mesenchyme to condense and ultimately form bony labyrinth. S = stapes, I =
incus, M = malleus.
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Fig. 12C. —Drawings reveal development of external, middle, and inner
ear. Gray area = cartilage condensations of neural crest origin, areas with
horizontal lines = ectoderm, areas with diagonal lines = endoderm. External
auditory canal (EAC) is separated from tympanic cavity (TC) by tympanic
membrane (TM), which has inner layer of endoderm, middle layer of mesoderm,
and outer layer of ectoderm. Tympanic cavity has expanded around ossicles,
leaving endodermal surface layer. Membranous labyrinth and surrounding bony
labyrinth are in apposition with tympanic cavity via oval window (OW) and
round window (RW). ES = endolymphatic sac, ED = endolymphatic duct, S =
saccule, CD = cochlear duct, U = utricle, AT = auditory tube, SSC = superior
semicircular canal, LSC = lateral semicircular canal, PSC = posterior
semicircular canal, ET = epitympanum.
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Fig. 13A. —Abnormal facial nerve course and small tympanic cavity in
5-year-old boy with left hemifacial microsomia. Coronal CT scan obtained
through normal right temporal bone shows horizontal segment of facial nerve
lying just beneath lateral semicircular canal (white arrowhead).
Stapes inserts into unobstructed oval window (black arrowhead).
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Fig. 13B. —Abnormal facial nerve course and small tympanic cavity in
5-year-old boy with left hemifacial microsomia. Coronal CT scan obtained
through abnormal left temporal bone shows anterior displacement of vertical
segment of facial nerve (arrows), which crosses in front of oval
window (arrowhead). Tympanic cavity measures less than 3 mm from
promontory of cochlea to lateral wall of tympanic cavity. Also note bony
atresia of external auditory canal and virtual aplasia of pinna.
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Otic Vesicle
During the latter part of the third week of gestation, the otic placode
forms as a surface thickening of the ectoderm overlying the rhombencephalon.
The placode subsequently invaginates to form the otic pit, before it pinches
off to form the otic vesicle
[2] (Fig.
12A,12B,12C).
The otic vesicle migrates in close proximity of the developing middle ear and
remodels into the complex membranous labyrinth. Concurrently the otic vesicle
induces the surrounding mesoderm to condense into the enveloping bony
labyrinth. Abnormalities of the membranous labyrinth and bony labyrinth seen
in patients with hemifacial microsomia include hypoplasia and atresia of the
oval and round windows and abnormal development of the cochlea and
semicircular canals [4].
Acknowledgments
We thank David W. Ehlert for preparing the medical illustrations.
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Introduction
Facial Musculoskeletal...
