Embryology, Anatomy, Normal Findings, and Imaging Techniques

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Chapter 13

Embryology, Anatomy, Normal Findings, and Imaging Techniques

Embryology of the Neck

Accurate diagnosis and successful treatment of congenital anomalies and masses of the neck are dependent on an understanding of the complex embryologic development of this region and the anomalies that result from abnormal development.

This chapter will focus on the embryology of the neck and the oral cavity. The embryology of the orbit, face and sinuses, temporal bone, and ear are addressed in Chapters 4, 8, 9, and 18.

Many of the structures of the head and neck form from an interaction between somitomeres, somites, the mesenchyme, and the branchial apparatus.

Development of the Mesoderm, Somitomeres, and Somites

After neurulation occurs, the mesoderm subdivides into the lateral, intermediate, and paraxial mesoderm. The lateral mesoderm forms most of the throat and larynx. The intermediate mesoderm does not form any part of the head and neck. The paraxial mesoderm forms the seven somitomeres and 42 to 44 paired somites. The five most rostral somites are involved in the formation of head and neck musculature (Fig. 13-1). The somitomeres and somites form before the development of the branchial apparatus.

The branchial apparatus, that is, the branchial arches, clefts, pouches, and membrane, begin to form late in the third week of gestation. The buccopharyngeal membrane breaks down and the mesodermal branchial bars begin to form six pairs of branchial arches. The fifth arch is rudimentary and disappears.

The fourth somitomere invades the first branchial arch and generates the formation of the muscles of mastication, that is, the masseter, pterygoid, and temporalis muscles. These muscles are innervated by the trigeminal nerve (CN V).

The seventh somitomere interacts with the third brachial arch to form the stylopharyngeus muscle, which is innervated by the glossopharyngeal nerve (CN IX).

The first four occipital somites invade the fourth and sixth brachial arches and thus stimulate the formation of the extrinsic and intrinsic laryngeal muscles innervated by the vagus nerve (CN X) and the cranial segment of the spinal accessory nerve (CN XI).

The third through seventh somites form the sternocleidomastoid muscle and trapezius and are innervated by the spinal accessory nerve (CN XI).

The intrinsic and extrinsic tongue muscles are likely derived from the second through fourth occipital somites and are innervated by the hypoglossal nerve (CN XII).

The contribution of the somitomeres and somites to the formation of muscles and their distinct innervation is unchanged throughout growth and development. Thus although many muscles migrate in location, their nerve supply is maintained and hence their branchial arch origin can always be identified (see Fig. 13-1).

Development of the Branchial Apparatus

Formation of the branchial apparatus occurs between the fourth through seventh weeks of development. The pharynx constitutes much of the foregut during the first few weeks of development. Formation of the five branchial arches (I, II, III, IV, and VI) results from the breakdown of the buccopharyngeal membrane and segmentation of the mesoderm. Migration of neural crest cells to this location stimulates growth and development. Each arch has its own outer epithelial lining of ectoderm separated by five clefts and an inner epithelial lining of endoderm with five corresponding pouches and a central cartilaginous core, which is a mesenchymal derivative that participates in the formation of the characteristic skeletal, muscular, ligamentous, vascular, and neural components of each arch.

Shortly after formation of the branchial arches, the first and second arches undergo mesodermal proliferation, thus creating the epicardial ridge, which contains the mesodermal precursor of the sternocleidomastoid, the trapezius, and the infrahyoid and lingual muscles. The nerves of the epicardial ridge are the hypoglossal (CN XII) and spinal accessory (CN XI) nerves. The proliferation of mesenchyme overgrows branchial arches II, III, and IV and narrows branchial clefts II, III, and IV. Subsequently, an ectodermal pit is formed—the cervical sinus of His—which obliterates with further development; failure of obliteration results in formation of branchial sinus, clefts, or cysts of types II, III, or IV.

Branchial Apparatus and its Contribution to the Structures of the Neck

Branchial Arches: The first branchial arch (Fig. 13-2) is composed of a dorsal segment known as the maxillary process and a ventral segment known as Meckel cartilage or the mandibular process; both involute. The ossification around Meckel cartilage is the precursor of the mandible and the sphenomandibular cartilage in the neck. The muscle derivatives of the first arch are the muscles of mastication (the masseter, pterygoid, and temporalis muscles), the tensor tympani and tensor veli palatine muscles, the anterior belly of the digastric muscle, and the mylohyoid muscle. The trigeminal nerve (CN V) provides motor and sensory innervation to the first branchial arch.

The second branchial arch is also known as Reichert cartilage. It gives rise to the upper body and lesser cornu of the hyoid bone, the styloid process, and stylohyoid ligament. The muscle derivatives include the platysma, the posterior belly of the digastric, and the stylohyoid. The nerve of the second brachial arch is the facial nerve (CN VII), which is primarily motor. The main sensory component is the chorda tympani branch that is carried with a branch of the trigeminal nerve (CN V3) to supply taste to the anterior two thirds of the tongue. The artery of the second brachial arch is the stapedial artery, which normally regresses aside from some contributions to the internal and external carotid arteries.

The third branchial arch cartilage derivatives include the greater cornu and inferior body of the hyoid. The muscle derivatives include the stylopharyngeus and superior and middle pharyngeal constrictors. The nerve of the third brachial arch is the glossopharyngeal nerve (CN IX). The neural crest cells of the third branchial arch also form the carotid bodies. The artery of the third branchial arch contributes to the common carotid artery and the internal and external carotid arteries.

The fourth and sixth branchial arch cartilage derivatives fuse to form the larynx and the laryngeal cartilages (the thyroid, cricoid, arytenoid, corniculate, and cuneiform). Muscle derivatives include the cricothyroid muscle, the levator veli palatini, and the inferior pharyngeal constrictors. The muscle derivatives of the sixth arch are the remaining intrinsic muscles of the larynx. The nerve of the fourth arch is the superior laryngeal nerve, and the nerve of the sixth arch is the recurrent laryngeal nerve. Both are branches of the vagus nerve (CN X). The artery of the fourth branchial arch contributes to the aortic arch on the left and the subclavian artery on the right. The artery of the sixth branchial arch becomes the ductus arteriosus and the pulmonary artery. Between the branchial arches lie the paired branchial pouches and clefts.

Branchial Pouches: The first branchial pouch does not contribute to the structures of the neck. The second branchial pouch gives rise to the palatine tonsils and tonsillar fossa. The third branchial pouch gives rise to the inferior parathyroids and thymus. The early embryologic connections to the pharynx normally are obliterated. The fourth branchial pouch gives rise to the superior parathyroid glands and the ultimobranchial body, which contains the parafollicular cells (C cells) of the thyroid gland. The fifth branchial pouch degenerates. The branchial clefts do not contribute to any neck structures and are obliterated as development occurs (Tables 13-1 and 13-2).

Table 13-1

Derivatives of the Branchial Arches

image

CN, Cranial nerve.

Adapted from Moore KL, Persaud MG, Torchia MG. Before we are born. Philadelphia: Saunders/Elsevier; 2008.

Table 13-2

Derivatives of the Branchial Pouches

Pouch Derivatives
First Eustachian tube, middle ear, portions of mastoid bone
Second Palatine tonsils, tonsillar fossa
Third Inferior parathyroids, thymus
Fourth and sixth Superior parathyroids, parafollicular cells of thyroid

Adapted from Moore KL, Persaud MG, Torchia MG. Before we are born. Philadelphia: Saunders/Elsevier; 2008.

Embryology of the Tongue

The tongue forms from the first four branchial arches. Two lateral and one central swelling, the tuberculum impar, form from the first branchial arch. A second central swelling, the copula/hypobranchial eminence, forms from the second, third, and fourth branchial arches. A third central swelling from the fourth branchial arch forms the epiglottis. Thus the anterior two thirds or body of the tongue forms from the first branchial arch, whereas the root of the tongue forms from the second, third, and fourth branchial arches. The groove that is formed where the anterior and posterior portions of the tongue fuse is called the terminal sulcus.

The hypoglossal nerve (CN XII) innervates all the intrinsic tongue muscles and all extrinsic tongue muscles but the palatoglossus. Sensory innervation is by the lingual branch of CN V3, the chorda tympani branch of CN VII, the lingual branch of CN IX, and the recurrent laryngeal branch of CN X.

Embryology of the Thyroid Gland

The thyroid gland originates from a median endodermal thickening in the floor of the primitive pharynx in the third to fourth week of development. The thyroid primordium develops between the tuberculum impar and the copula of the first and second pouches. The foramen cecum is the remnant of the thyroid promordium in this location, between the anterior two thirds and the posterior one third of the tongue. The thyroid gland passes anterior to the hyoid and laryngeal cartilages and descends anterior to the thyrohyoid membrane and the strap muscles. The thyroid gland reaches its final position by the seventh week of development. During its inferior migration, the thyroid anlage is connected to the tongue by the normally transient thyroglossal duct. Innervation of the thyroid gland is primarily by the sympathetic middle cervical ganglion.

Embryology of the Salivary Glands

The common pathway for salivary gland development is the ingrowth of surface epithelium (primarily ectoderm, but also endoderm for minor salivary gland formation) into the underlying mesenchyme.

The precursors of the parotid gland appear between the fourth to sixth weeks of gestation, and the submandibular and sublingual glands appear between the sixth to eighth weeks of gestation. The minor salivary glands do not develop until the twelfth week of gestation.

A process of proliferation, division, and canalization occurs. Interaction with and stimulation by the autonomic nervous system is essential for normal salivary gland development and function. The final process of encapsulation occurs in reverse to the order of development and growth. Encapsulation of the parotid gland occurs after formation of the lymphatic system, accounting for the presence of intraparotid lymph nodes.

The parotid gland is innervated by CN IX, the submandibular and sublingual glands are innervated by CN VII, and the minor salivary glands are innervated by CN V.

Anatomy of the Neck

Clinical evaluation and classic anatomy divides the neck into triangles. The largest are the anterior and posterior triangles, which are defined and separated by the sternocleidomastoid muscles. The anterior triangle is further subdivided into the paired carotid and submandibular triangles (separated by the posterior belly of the digastric muscle) and the single midline submental and infrahyoid muscular triangles. The posterior triangle consists of the paired occipital and subclavian triangles, which are separated by the inferior belly of the omohyoid muscle (Fig. 13-3). The central cavity is divided into the nasopharynx, oropharynx, hypopharynx, and oral cavity.

This approach to neck anatomy does not reflect anatomy as defined by the fascial layers, that is, the superficial and deep cervical fascia of the head and neck. The deep cervical fascia is composed of three layers:

The advent of cross-sectional imaging enabled a new approach to neck anatomy defined by the concept of dividing the neck into the suprahyoid and infrahyoid compartments, with further subdivision of each compartment into fascially defined spaces (Figs. 13-4 and 13-5). The resultant refined approach to differential diagnosis, combined with the use of surgically and pathologically defined common terminology and nomenclature, has improved communication between radiologists and clinicians.

The pharyngeal mucosal space, which is located in the suprahyoid neck, is the surface of pharynx. It encompasses the nasopharyngeal, oropharyngeal, and hypopharyngeal mucosa. Centrally located, it is posterior to the retropharyngeal space and lateral to the parapharyngeal space. It is not a true fascially enclosed space because only its deep margin is bound by the ML-DCF.

The parapharyngeal space is located in the suprahyoid neck; it extends from the skull base to the submandibular space. The medial fascial boundary is the visceral/buccopharyngeal fascia. The pterygomandibular raphe and masticator space is its anterior boundary. Laterally and posteriorly it is bounded by the carotid and retropharyngeal space.

The carotid space, which is located in both the suprahyoid and infrahyoid neck, extends from the skull base to the aortic arch. All three layers of deep cervical fascia form the carotid sheath. The carotid sheath is better defined in the infrahyoid neck and more loosely formed in the suprahyoid neck.

The retropharyngeal space, which is located in both the suprahyoid and infrahyoid neck, extends from the skull base to T3. The ML-DCF constitutes the anterior wall, and the DL-DCF constitutes the posterior wall. The lateral wall is the alar fascia, a small fragment of the DL-DCF. It is posterior to the pharyngeal mucosal space in the suprahyoid neck and the visceral space in the infrahyoid neck, anterior to the danger space posterior, and medial to the carotid space.

The masticator space, which is located in the suprahyoid neck, extends from the superior aspect of suprazygomatic masticator space/temporal fossa at the level of parietal bone to the inferior aspect of the infrazygomatic masticator space/undersurface of the posterior body of the mandible. It is bounded by a sling of the SL-DCF that extends from the inferior mandible to the skull base and zygomatic arch. It is anterior to the parotid space, anterolateral to the parapharyngeal space, and lateral to the pharyngeal mucosal space. Superior to it is the skull base, including the foramina ovale and spinosum.

The parotid space, which is located in the suprahyoid neck, extends superiorly from the external auditory canal and mastoid tip to below angle of mandible. It is enclosed by the SL-DCF.

The perivertebral space, which is located in both the suprahyoid and infrahyoid part of the neck, extends from the skull base to T4 and consists of a prevertebral and a paraspinal component. It is enveloped by the DL-DCF. The perivertebral space is posteromedial to the carotid space and medial to the posterior cervical space.

The visceral space, which is located in the infrahyoid neck, lies anterior to the retropharyngeal space in the midline and is enclosed by the ML-DCF.

The posterior cervical space extends from the mastoid tip to the level of the clavicle. Its superficial boundary is the SL-DCF, and its deep boundary is the deep cervical DL-DCF. It lies posterior to the carotid sheath, posteromedial to the sternocleidomastoid muscle, and anterolateral to the paraspinal component of the perivertebral space (Tables 13-3 and 13-4).

Table 13-3

Anatomic Spaces of the Suprahyoid Neck

Space Contents
Pharyngeal mucosal space Mucosa, minor salivary glands and lymphoid tissue, pharyngobasilar fascia, buccopharyngeal fascia, superior and middle pharyngeal constrictor muscles, levator veli palatini muscle, cartilaginous end of eustachian tube (torus tubarius)
Parapharyngeal space (prestyloid parapharyngeal space) Deep portion of parotid gland, minor salivary glands, pterygoid venous plexus, internal maxillary artery, ascending pharyngeal artery, branches of cranial nerve V3, cervical sympathetic chain and fat
Carotid space (retrostyloid parapharyngeal space) Internal carotid artery, internal jugular vein, cranial nerves IX-XII, sympathetic chain, lymph nodes—deep cervical chain
Retropharyngeal space Fat, lymph nodes—retropharyngeal (medial and lateral)
Masticator space Ramus and posterior body of mandible, muscles of mastication—pterygoid, masseter, and temporalis; mandibular division trigeminal nerve (V3)—inferior alveolar and lingual nerves, inferior alveolar vein and artery, pterygoid venous plexus
Parotid space Parotid gland and duct, cranial nerve VII, external carotid artery, retromandibular vein, lymph nodes—intraparotid and periparotid
Perivertebral space Prevertebral muscles, scalene muscles, vertebral artery and vein, brachial plexus, phrenic nerve
Vertebral bodies and discs

Adapted from Som PM, Curtin HD. Head and neck imaging. 4th ed. St Louis: Mosby; 2003.

Table 13-4

Anatomic Spaces of the Infrahyoid Neck

Space Contents
Visceral space Larynx, hypopharynx and cervical esophagus, trachea, thyroid gland, parathyroid glands, lymph nodes, recurrent laryngeal nerve (branch cranial nerve X), third and fourth branchial apparatus and thyroid/parathyroid anlage remnants
Retropharyngeal space Fat, remnants of third branchial apparatus
Carotid space Common and internal carotid arteries, internal jugular vein, cranial nerve X, sympathetic chain, lymph nodes, carotid body, second branchial apparatus remnants
Perivertebral space Prevertebral, scalene, and paraspinal muscles, brachial plexus, phrenic nerve, vertebral artery and vein
Vertebral bodies and discs
Anterior cervical space Extension of submandibular space of suprahyoid neck
Composed of fat
Posterior cervical space Cranial nerve XI, spinal accessory nodes, preaxillary brachial plexus, fat

Anatomy of the Oral Cavity

The oral cavity is located anterior to the oropharynx. It is separated from the oropharynx by the soft palate, anterior tonsillar pillars, and circumvallate papillae. The mylohyoid muscle separates the lower oral cavity into the submandibular and sublingual spaces and forms the floor of the mouth, arising from the mandible and attaching to the hyoid.

The submandibular space, which is located inferior and lateral to the mylohyoid muscle and superior to the hyoid bone, is enveloped by the SL-DCF. Posteriorly no fascial separation is found between the submandibular space, the sublingual space, and the inferior parapharyngeal space.

The sublingual space, which is located superior and medial to mylohyoid muscle and lateral to genioglossus-geniohyoid muscle complex, is not enclosed by fascia (Table 13-5).

Table 13-5

Contents of the Submandibular and Sublingual Spaces

Space Contents
Submandibular Submandibular gland, submandibular and submental lymph nodes, facial artery and vein, inferior cranial nerve XII, anterior belly of digastric muscle
Sublingual Hyoglossus muscle (anterior margin), lingual nerve (sensory branches of cranial nerve V3 and the chorda tympani branch of cranial nerve VII), distal cranial nerve IX and cranial nerve XII, lingual artery and vein, sublingual gland and duct, deep portion of the submandibular gland and duct

Imaging Techniques

Cross-sectional imaging has become an integral tool in the diagnosis, characterization, and staging of neck pathology. Each modality has its strengths and drawbacks. The modalities chosen depend on the clinical question to be answered and the patient’s clinical presentation and condition. In a given situation, one modality may suffice or a combination may be required to provide a diagnosis and to assist in planning treatment, as well as to provide assessment of disease progression or treatment efficacy.

Ultrasonography should always be considered because it is readily available, relatively inexpensive, and uses no ionizing radiation. High-frequency linear array transducers provide optimal spatial resolution, although sector or curved array transducers can be useful to image deeper neck structures. Ultrasound readily differentiates cystic from solid lesions, and Doppler imaging can determine vascularity. Additionally, ultrasound is valuable in guiding interventions such as aspiration or biopsy.

Computed tomography (CT) is extremely useful in evaluating neck pathology. New multidetector scanners provide rapid scan times, resulting in diminished motion artifact and little need for sedation. Volumetric thin-section acquisitions allow multiplanar and three-dimensional reconstructions, which can aid in the detection and display of abnormalities. Drawbacks include ionizing radiation and the need for iodinated contrast material. As with all CT studies, the imaging protocol and radiation dose should be tailored for patient size and desired image quality.

Magnetic resonance imaging (MRI) allows exquisite delineation of anatomy and pathology, with superior soft tissue contrast resolution relative to CT. MRI allows direct acquisition in any desired anatomic plane and does not expose patients to ionizing radiation. However, many younger patients require sedation for this procedure, and patients with implants that are not compatible with MRI may not be candidates. A combination of T1-weighted, T2-weighted, inversion recovery, and other sequences can help delineate different tissue types. Angiographic techniques are useful to better delineate the vasculature.

Positron emission tomography using fluorine-18 fluorodeoxyglucose is not a first-line imaging modality, but it is valuable in the assessment of neck masses. It is sensitive for the detection of increased glucose metabolism, which often is present with malignancy. Differentiation between physiologic uptake, posttreatment uptake, and pathologic uptake is critical; standard uptake values should be used. Spatial resolution is relatively poor, but acquisition of images with concurrent CT or MRI, or fusion of positron emission tomography studies with recent CT or MRI, allows more precise anatomic localization of areas of abnormal uptake.

Key Points

Suggested Readings

Dolinskas, CA. ACR-ASNR practice guidelines for the performance of magnetic resonance imaging (MRI) of the head and neck [online publication]. Reston, VA: American College of Radiology; 2012.

Harnsberger, HR, Wiggins, RH, III., Hudgins, PA, et al. Diagnostic imaging head and neck, part III. Salt Lake City: Utah: Amirys Inc; 2004.

Jinkins, JR. Atlas of neuroradiologic embryology, anatomy, and variants. Philadelphia: Lippincott Williams & Wilkins; 2000.

Ludwig, BJ, Foster, BR, Saito, N, et al. Diagnostic imaging in nontraumatic pediatric head and neck emergencies. Radiographics. 2010;30(3):781–799.

Mafee MF, Valvassori GE, Becker M, eds. Imaging of the head and neck, 2nd ed, New York: Thieme Stuttgart, 2004.

Moore, K, Persaud, TVN. Before we are born: essentials of embryology and birth defects, 7th ed. Philadelphia: Saunders; 2008.

Mukherji, SK, Wippold, FJ, II., Cornelius, RS, et al. ACR Appropriateness Criteria neck mass/adenopathy [online publication]. Reston, VA: American College of Radiology; 2009.

Siegel, MJ. Pediatric sonography, 4th ed. Philadelphia: Lippincott Williams & Wilkins; 2010.

Som, PM, Curtin, HD. Fascia and spaces of the neck. In Som PM, Curtin HD, eds.: Head and neck imaging, 4th ed, St Louis: Mosby, 2003.

Som, PM, Smoker, WRK, Balboni, A, et al. Embryology and anatomy of the neck. In Som PM, Curtin HD, eds.: Head and neck imaging, 4th ed, St Louis: Mosby, 2003.

Weiss, KL, Cornelius, RS, Greeley, AL, et al. Hybrid convolution kernel: optimized CT of the head, neck, and spine. AJR Am J Roentgenol. 2011;196(2):403–406.

Wippold, FJ, 2nd. Head and neck imaging: the role of CT and MRI. J Magn Reson Imaging. 2007;25(3):453–465.

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