Author’s Accepted Manuscript

Chapter 1. Neck Anatomy, Imaging Based Level

Nodal Classification and Impact of Primary Tumor
Site on Patterns of Nodal Metastasis

Matthew H. Kulzer, Barton F. Branstetter

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DOI: http://dx.doi.org/10.1053/j.sult.2017.05.002
Reference: YSULT755
To appear in: Seminars in Ultrasound, CT, and MRI
Cite this article as: Matthew H. Kulzer and Barton F. Branstetter, Chapter 1.
Neck Anatomy, Imaging Based Level Nodal Classification and Impact of
Primary Tumor Site on Patterns of Nodal Metastasis, Seminars in Ultrasound,
CT, and MRI, http://dx.doi.org/10.1053/j.sult.2017.05.002
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Chapter 1. Neck Anatomy, Imaging Based Level Nodal Classification and Impact of Primary

Tumor Site on Patterns of Nodal Metastasis

Name, degree, professional affiliation: Matthew H. Kulzer, MD

Barton F. Branstetter IV, MD, FACR

Institution: University of Pittsburgh Medical Center

Acknowledgement of grant: No grant funding was utilized

Contact info: branbf@upmc.edu, kulzermh@upmc.edu

Corresponding author: branbf@upmc.edu

Abstract

The anatomy of the neck is complex, with many critical structures crowded together in a

relatively small cross sectional area. Many structures in the neck also have similar soft tissue density or

signal which further complicates interpretation for the radiologist, who relies on tissue differences to

create contrast resolution and distinguish structures. Head and neck cancer incidence worldwide

exceeds 550,000 cases per year with diagnosis, treatment, and prognosis relying highly on a thorough

knowledge of this compact space. This chapter will focus on reviewing head and neck anatomy with

special attention to nodal anatomy and discussing the expected patterns of nodal spread in head and

neck cancers.

Introduction

Although the head and neck accounts for only 20% of the body’s volume, it contains 40% of the

body’s lymph nodes.1,2 Surrounded by fat, normal head and neck lymph nodes can be difficult to identify

on imaging and at the time of surgery.2 Thus, the anatomy of the lymphatic system in the head and neck

can be a challenge for both radiologists and clinicians.

The annual incidence of head and neck cancers worldwide exceeds 550,000 cases with around

300,000 deaths per year.3 Depending on the primary site, up to 80% of patients with upper

aerodigestive mucosal malignancy will have cervical nodal metastases at presentation.4 Given the

impact of nodal disease on both treatment and prognosis, it is crucial for radiologists to be familiar with
cervical nodal anatomy, nodal classification, and tumor spread patterns to effectively communicate with

both head and neck surgeons and pathologists.

This chapter will begin by reviewing nodal anatomy in the neck using easily-identified imaging

landmarks. The normal appearance of lymph nodes and the expected patterns of nodal spread from

head and neck cancers will be discussed.

Neck Anatomy

Landmarks

The neck has been described as a cylinder with the vertebral column and its surrounding

musculature occupying the posterior half of the cylinder and the cervical viscera (the pharynx, larynx,

esophagus, trachea, and parathyroid and thyroid glands) within the anterior half of the cylinder.5

Classically, clinicians divide the neck into triangles using superficial musculature that is readily identified

on physical exam.5 With cross sectional imaging, radiologists are able to evaluate the deep structures of

the neck in greater detail, dividing the neck into compartments separated by layers of cervical fascia.

Cervical structures readily identified on cross sectional imaging can serve as landmarks both in the

evaluation of primary tumors of the head and neck, but also in classifying the level of lymph node

involvement.
Bones and Cartilages

The hyoid bone is a horseshoe-shaped structure positioned in the anterior midline neck just

below the mandible where the neck begins to assume a cylinder shape. The hyoid bone lies in the

transverse plane and is comprised of five segments -- a central body, two greater cornua projecting

posterolaterally from each end of the body, and two lesser cornua extending upward from the junction

of the body and greater cornua (Fig 1). A radiolucent or radiodense line may (or may not) be seen on

computed tomography (CT) at the junction of the body and greater cornua on the anterolateral aspect

of either side of the normal hyoid bone. This finding is often asymmetric.5

The thyroid cartilage is the largest of the laryngeal cartilages and lies in the anterior midline

neck below the hyoid bone. It consists of two alae (or wings) which merge in the midline to form a ridge

known as the laryngeal prominence (Fig 2). Even more than most cartilages, the thyroid cartilage ossifies

in young adulthood. On CT, the ridged configuration of the laryngeal prominence can help distinguish an

ossified laryngeal cartilage from the relatively rounded or flat anterior surface of the hyoid bone.

The cricoid cartilage is smaller, but thicker and stronger than the thyroid cartilage. Forming the

lower and posterior walls of the larynx, it is located just below the thyroid cartilage (see Fig 2). The

cricoid cartilage consists of two parts -- a posterior quadrate lamina and a narrow anterior arch. With its

posterior lamina, it forms the only complete cartilage ring in the upper airway.

Muscles

The major muscles groups in the neck are used to divide the neck into triangles on physical

examination (Fig 3). The digastric muscle consists of two muscular bellies united by a rounded or central

intergastric tendon. The anterior belly arises from a depression on the inner surface of the lower

mandible near the midline. Extending posteriorly and inferiorly along the lateral margin of the hyoid
bone, it continues as the central tendon which is held in place by a fibrous loop along the side of the

greater cornu of the hyoid bone (see Fig 1). The posterior belly of the digastric muscle is longer than the

anterior belly and continues posteriorly and superiorly from the central tendon to attach to the medial

surface of the mastoid process of the temporal bone.

The sternocleidomastoid muscle is a thick, round muscle which extends obliquely across the side

of the neck, arising from the sternum and clavicle by two heads and inserting on the lateral surface of

the mastoid process. Given its prominence in the lateral neck, it is a commonly-used landmark not only

in the image-based classification of lymph nodes, but also clinically in dividing the neck into triangles.

The trapezius muscle is a superficial, flat, triangular muscle extending longitudinally from the

occipital bone to span the cervical and thoracic vertebrae and drape over the shoulders. Laterally, it

attaches to the spine of the scapula, acromion, and clavicle.

The infrahyoid muscles (commonly known as the strap muscles) include the sternohyoid,

omohyoid, sternothyroid, and thyrohyoid muscles.6 Covering the front and sides of the larynx, trachea,

and thyroid gland, they are a group of four thin, flat muscles that protect the cervical viscera and

suspend the larynx. 6 They can be difficult to distinguish individually on imaging. The sternohyoid muscle

is the most superficial, lying on each side of the midline, ascending from an origin on the posterior

surface of the manubrium sterni and the sternal end of the clavicle, and inserting above the body of the

hyoid bone.6 Similar to the digastric muscle, the omohyoid consists of two fleshy bellies united by an

intergastric central tendon. Arising from the upper border of the scapula, the inferior belly forms a

small, flat muscle which extends anteriorly and slightly superiorly posterior to the sternocleidomastoid

muscle to form the central tendon. The central tendon is held in position by a process of the deep

cervical fascia, anchoring it to the clavicle and first rib. The superior belly projects from the central

tendon almost vertically to attach to the lower border of the hyoid bone. The sternothyroid muscle
originates from the posterior surface of the manubrium sterni just below the sternohyoid muscle, as

well as from the edge of the first (and occasionally second) rib cartilage. It courses just deep to the

sternohyoid muscle, covering the thyroid gland, and inserting on the lamina of the thyroid cartilage. The

thyrohyoid muscle is a small, quadrilateral muscle arising from the lamina of the thyroid cartilage and

coursing superiorly to insert on the greater cornu of the hyoid bone.

Vessels

The common carotid arteries differ in length and origin with the left common carotid artery

typically branching directly from the aortic arch and the right common carotid artery branching from the

innominate artery. Each vessel courses obliquely upward from behind the sternoclavicular articulation,

typically bifurcating at the level of the upper border of the thyroid cartilage. There are usually no

branches of the common carotid arteries until their bifurcation into the external and internal carotid

arteries. At the bifurcation, the internal carotid artery lies posterolateral to the external carotid artery

(Fig 4). The internal carotid artery courses upward toward the skull base, accompanied by the internal

jugular vein, which is located medial to the artery, and the sympathetic trunk, which is located anterior

to the artery. The external carotid artery travels anteriorly and superiorly at the common carotid

bifurcation and has eight major branches (superior thyroid, lingual, ascending pharyngeal, occipital,

facial, posterior auricular, internal maxillary, and superficial temporal arteries) that predominantly

supply the extracranial head and neck with several branches supplying intracranial structures (e.g., the

middle meningeal artery, a branch of the internal maxillary artery, supplies portions of the dura mater).

The vertebral artery typically arises as the first branch from the subclavian artery, ascending

through the foramina transversaria in the transverse processes of the first six cervical vertebrae before

winding around the atlas and entering the skull base.

 The internal jugular vein is a direct continuation of the transverse sinus via the sigmoid sinus and

jugular bulb. It courses inferiorly along the lateral aspect of the internal carotid artery then along the

lateral aspect of the common carotid artery before joining with the subclavian vein to form the

innominate vein. The external jugular vein receives the greater part of the blood from the extracranial

and deep facial structures, forming at the junction of the posterior division of the posterior facial and

posterior auricular veins at the level of the angle of the mandible within the substance of the parotid

gland. It courses inferiorly and obliquely between the sternocleidomastoid and platysma muscles and

joins the subclavian vein to form the innominate vein anterior to the anterior scalene muscle. The

anterior facial vein lies along the anterolateral surface of the submandibular gland between the gland

itself and adjacent lymph nodes. The vein is a useful landmark that will separate the gland from adjacent

lymphadenopathy, but will be displaced by masses arising within the gland itself (Fig 5).5,7

The thoracic duct drains a majority of the body’s lymph into the bloodstream.8 It is a common

trunk of all the lymph vessels, with the exception of those that drain the right upper extremity, right side

of the head, neck, and thorax, right lung, right heart, and hepatic dome.9 The thoracic duct is formed by

the cisterna chyli, the lower two thirds of the right lymphatic trunk, and the upper third of the left

lymphatic trunk.8 Its typical course (seen in 60-70% of individuals) involves crossing to the left at the

level of the fourth thoracic vertebral body, ascending adjacent to the vertebral column behind the

esophagus, and passing behind the carotid sheath and its contents, superficial to the anterior scalene

muscle.6,8 The thoracic duct then forms an arch 3-5 cm above the clavicle, angling forward posterior to

the left common carotid artery, and terminating at the confluence of the internal jugular and left

subclavian veins.6,8 The thoracic duct is frequently visible on cross-sectional imaging.8

Triangles

Classically, the quadrilateral shape created by the neck musculature has been organized on

physical examination into two large triangles separated by the sternocleidomastoid muscle. The

traditional classification for cervical lymph nodes, described by Rouviere in 1938, which was the

continuation of the work of several anatomists in the early 1900s, used these triangles as the basis for

naming nodal clusters and chains.1,2

The anterior triangle is bounded medially by the midline neck and laterally by the anterior

margin of the sternocleidomastoid muscle with its base along the inferior margin of the mandible and its

apex at the sternum. The hyoid bone and posterior belly of the digastric divide the anterior triangle into

suprahyoid and infrahyoid regions.

The anterior triangle can be further subdivided into four smaller triangles by the digastric

muscle and the superior belly of the omohyoid muscle (Fig 6). The anterior belly of the digastric muscle

divides the suprahyoid region into the paired submandibular triangles laterally and the submental

triangle medially.

The submental triangle contains a cluster of lymph nodes and small branches of the facial artery

and vein. Occasionally, these small venous branches will join at the level of the hyoid bone to form the

anterior jugular vein.10

The submandibular triangle, sometimes referred to as the digastric triangle, is separated from

the submental triangle by the anterior belly of the digastric muscle. The anterior portion contains the

submandibular gland while the posterior portion contains the external carotid artery and its branches. A

cluster of lymph nodes lies anterolateral to the gland, along with the mylohyoid nerve and branches of

the facial artery.

 The carotid triangle occupies the infrahyoid portion of the anterior triangle and is so named

because the common carotid artery can be palpated within it. It can be further subdivided into the

superior carotid triangle and inferior carotid triangle by the superior belly of the omohyoid muscle.

The posterior triangle is bounded anteriorly by the sternocleidomastoid muscle and posteriorly

by the trapezius muscle with its base along the superior margin of the clavicle and its apex at the

occipital bone. It can be further subdivided into the occipital triangle (superiorly) and subclavian triangle

(inferiorly) by the inferior belly of the omohyoid muscle (see Fig 6). The larger occipital triangle contains

the spinal accessory nerve and the upper part of the brachial plexus. Chains of lymph nodes course both

along the posterior margin of the sternocleidomastoid muscle and along the course of the spinal

accessory nerve within the occipital triangle. The smaller subclavian triangle contains the lower portions

of the brachial plexus as well as portions of the subclavian artery, the transverse cervical artery, and a

chain of lymph nodes extending along the transverse cervical artery.

Nodal Appearance on Imaging

A single lymph node metastasis from a head and neck squamous cell carcinoma portends a five-

year-survival rate of 50% and an additional contralateral lymph node metastasis further reduces survival

to 33%.11 Detecting pathologic nodes is therefore crucial to prognosis, as well as assisting in guiding

treatment.

Normal lymph nodes on CT have a homogeneous density close to that of muscle with smooth

margins and an oval or reniform configuration (Fig 7A).2,5 Similarly, on unenhanced T1-weighted MRI,

normal lymph nodes have a low-to-intermediate intensity close to muscle (Fig 7B).2,5 On T2-weighted

MRI images, however, normal lymph nodes demonstrate a signal intensity higher than muscle (Fig 7C).5
Following contrast administration, normal lymph nodes enhance homogeneously and to a greater

degree than muscle on both CT and MRI.5

The imaging characteristics of pathologic lymph nodes is further discussed in chapter 2, but

briefly, the most commonly used criteria for distinguishing metastatic from reactive nodes include size

and presence of central nodal necrosis.2 While in most other areas of the body, size is the favored

metric to distinguish between normal and pathologic lymph nodes, evaluating abnormal nodes by size is

the head and neck is confusing due to the wide range of reported normal sizes. In the literature, normal

sizes have been described as ranging from 7 mm to 3 cm.12,13,14 By convention, jugulodigastric and

submandibular nodes less than 15 mm in maximum longitudinal dimension, retropharyngeal nodes less

than 8 mm, and all remaining cervical nodes less than 10 mm in maximum longitudinal dimension, are

considered normal.4,15 However, at pathology 20% of nodes exceeding 10 mm contain no metastatic

deposits and histologically show only hyperplasia.4 Size alone cannot be relied upon to identify

pathologic nodes. Extracapsular tumor extension has been found in 23-25% of metastatic nodes less

than 10 mm in size.15,16 Node configuration is a feature exquisitely assessed by imaging to further

increase the sensitivity for identifying pathology. Normal lymph nodes on both CT and MR are reniform

in configuration with well-demarcated borders and a central hilum containing fat.5,9 Metastatic nodal

disease can manifest as alteration in this normal nodal configuration, with pathologic nodes assuming a

more rounded or irregular shape. Metastasis can result in replacement of the normal fat-containing

hilum with soft tissue.14 An asymmetric grouping of normal-sized nodes, or three or more contiguous

and confluent nodes along the drainage pathway of a primary tumor, should be viewed with a high

degree of suspicion (Fig 8).15 Nodal necrosis has been described as the most specific sign of metastatic

disease, with a specificity between 95 and 100%, and its appearance and mimics on imaging are further

discussed in chapter 2.17

Node Classification

Historically, the most common classification system for cervical lymphadenopathy was the

anatomically-based scheme described by Rouviere in 1938.18 Cervical lymph nodes are arranged in

clusters and chains, each of which has a characteristic drainage pattern.5 Clusters were named for the

fascial space which they occupy (e.g., submandibular nodes could be found within the submandibular

space).5 Chains were described by the structures which they accompanied (e.g., internal jugular nodes

could be found along the course of the internal jugular vein).5 In 1981, Shah,et al, recommended an

updated system organizing the cervical nodes into levels commonly encountered at the time of

surgery.19 In 1991 and again in 1998, the American Academy of Otolaryngology--Head and Neck Surgery

revised the classification system to more closely approximate revisions made to the American Joint

Commission on Cancer staging system for head and neck cancers, as well as to standardize terminology

used during head and neck dissections.20–22 This section will focus on the imaging-based nodal

classification described by Som, et al, which was designed to be used as an adjunct to the AJCC

classification, and is the most commonly used system by radiologists and clinicians in the management

of patients with nodal disease or head and neck cancer.21 In this system, the lymph nodes of the neck

are divided into 7 surgical levels (Fig 9).

Level I encompasses the nodes below the jaw: cranial to the hyoid bone, caudal to the

mylohyoid muscles, and anterior to a transverse line drawn through the posterior edge of the

submandibular gland on axial images.21,18 These nodes can also be referred to as submental and

submandibular lymph nodes with the submental nodes lying between the anterior bellies of the

digastric muscles and the submandibular nodes between the anterior and posterior bellies of the
digastric muscle on either side.5 The nodes can alternatively be divided into level Ia (submental nodes)

and Ib (submandibular nodes) (Fig 10).23

Level II, also referred to as upper jugular nodes, comprises the upper one third of the internal

jugular chain lymph nodes and the superior one half of the spinal accessory chain nodes.5 On imaging,

level II includes all lymph nodes bounded cranially by the skull base, laterally by a transverse line

through the posterior border of the sternocleidomastoid muscle on axial images, medially by the lateral

border of the strap muscles, and caudally by the carotid bifurcation, with the caudal margin of the hyoid

bone serving as an imaging landmark for the approximate location of the carotid bifurcation (Fig

11).5,21,22 Nodes within 2 cm of the skull base, medial to the internal carotid artery are not included in

level II and instead are classified as retropharyngeal nodes (Fig 12).21,22 As with level I, level II can further

be subdivided using the internal jugular vein as a landmark. Level IIa (previously described as upper

internal jugular) lymph nodes are all nodes within the above-described borders that are anterior,

medial, or lateral to the internal jugular vein, or inseparable from the internal jugular vein by a fat

plane.21,22 Level II nodes posterior to the internal jugular vein with a clear fat plane separating node from

vein are subclassified as level IIb nodes (previously described as upper spinal accessory nodes).21,22

Level III nodes represent those in the middle one third of the internal jugular chain.5 The

boundaries of level III are the caudal margin of the hyoid bone superiorly, the lower margin of the

cricoid cartilage inferiorly, the posterior border of the sternocleidomastoid muscle laterally, and the

medial margin of the internal carotid or common carotid arteries medially.5,21,22 In contrast to level II, in

which nodes medial to the medial margin of the internal carotid artery are named as retropharyngeal

nodes, nodes lying medial to the internal carotid (or common carotid) arteries below the caudal margin

of the hyoid bone are classified as level VI (above the top of the manubrium) or level VII (below the top

of the manubrium) nodes.

 The lower jugular group lymph nodes are located in level IV.5 The boundaries of level IV include

the lower margin of the cricoid cartilage superiorly, the level of the clavicle on axial images inferiorly, an

oblique line drawn between the posterior edge of the sternocleidomastoid muscle and the lateral

posterior edge of the anterior scalene muscle on axial images laterally, and the medial margin of the

common carotid artery medially.5,21,22 Lymph nodes medial to the medial margin of the common carotid

artery are classified in level VI, while nodes between the medial margin of the common carotid artery

and an oblique line drawn between the posterior edge of the sternocleidomastoid muscle and lateral

posterior edge of the anterior scalene muscle are classified in level IV (Fig 13).21,22 Virchow’s node, which

may be involved in head and neck, chest, or abdominal metastatic disease, is located in level IV and is

usually affected on the left (Fig 14).5,23

Level V nodes, located in the posterior triangle, are bounded by the skull base superiorly, the

posterior border of the sternocleidomastoid muscle anteriorly, the anterior edge of the trapezius muscle

posteriorly, and the clavicle inferiorly.21,22 This level has classically been described as containing the

nodes within the inferior half of the spinal accessory chain and the entirety of the transverse cervical

chain.5 Level V can further be subdivided into levels Va and Vb. Level Va nodes (spinal accessory chain)

lie between the skull base and lower margin of the cricoid cartilage and level Vb lymph nodes

(transverse cervical chain) located between the lower margin of the cricoid cartilage and the clavicle.21,22

Level VI nodes are located inferior to the lower margin of the hyoid bone, superior to the

manubrium, and between the internal or common carotid arteries.21,22 These were classically described

as visceral or juxtavisceral nodes and comprised the prelaryngeal, prethyroid, pretracheal, and

paratracheal chains.5 This includes the precricoid lymph node (Delphian node), as well (Fig 15).23
 Level VII nodes are those nodes caudal to the superior margin of the manubrium in the superior

mediastinum between the left and right common carotid arteries.21,22 The inferior margin is the

innominate vein. Level VII nodes are included in other classification schemes for chest lymph nodes.

There are several named lymph nodes which are not included in the above level-based system,

but instead are simply referred to by their anatomic descriptor. These include the retropharyngeal,

parotid, facial, occipital, and posterior auricular nodes (Fig 16).21,22 Supraclavicular lymph nodes are

occasionally named separately as well, but are actually incorporated into either levels IV or Vb.

Lymphatic flow from the head and neck proceeds to a pair of large lymph vessels, the jugular trunks,

which are lateral to the internal jugular veins.5 The left jugular trunk empties into the thoracic duct,

while the right jugular trunk empties directly into the right subclavian vein.5 Although they are large

relative to other lymphatic channels, the jugular trunks are usually not visible on imaging.

Patterns of Nodal Spread

The presence of metastatic lymph nodes at the time of initial presentation is the strongest

predictor for recurrence of nodal metastases and eventual distant metastases.2 Additionally, the

presence of a solitary ipsilateral or contralateral positive lymph node, or extracapsular spread of tumor,

each reduce the expected survival by approximately 50% for nearly all head and neck cancers.2 Most

mucosal head and neck tumors have a predictable pattern of metastasis.24 Knowledge of the lymphatic

drainage pathways is crucial not only to predict the pattern of disease spread and help focus both

clinical and imaging evaluation, but also in the evaluation of patients with metastatic lymphadenopathy

in whom the primary tumor is not clearly seen.

 Level I is the drainage site for anterior oral carcinomas, as well as lip, facial, and sinonasal

carcinomas.24 Level I nodes may also receive lymph from the floor of mouth, anterior tonsillar pillar,

eyelids and conjunctiva, anterior nose, and sublingual and submandibular glands.2

Level II is the most frequently involved nodal level in the neck.24 Metastatic involvement can

spread from primary tumors located in the pharynx, oral cavity, floor of mouth, palatine tonsil, tongue,

supraglottic larynx, parotid gland, or eye.2,24 Anterior oral carcinomas may also develop metastatic

lymphadenopathy in level II or III.24

Lymph nodes in level III are in the primary echelon drainage pathway for tumors of the

hypopharynx, glottic and supraglottic larynx, and thyroid gland.2,24 Level III nodes can also be involved in

tumors originating from the pharynx, oral cavity, floor of mouth, tongue, palatine tonsil, and parotid

gland.2 Metastases in Level II can spread inferiorly to Level III and from there to Level IV.

Level IV nodes are rarely the solely involved nodes in head and neck primary tumors.24 When

involved, primary sites include the subglottic larynx, thyroid gland, cervical esophagus, or an

infraclavicular primary (e.g., breast, lung, or gastric metastases).2,24 Occasionally, tonsillar primaries or

tumors of the occipital scalp may also spread to level IV primarily.2

Level V is commonly involved in advanced nodal disease from squamous cell carcinoma.24

Drainage to level V can be seen more frequently in nasopharyngeal carcinoma or skin cancers of the

occipital scalp or neck.24 Occasionally, tumor primaries in the posterior tongue, palatine tonsil,

hypopharynx, or parotid gland may spread to level V primarily.2

The Delphian node, which is a named level VI prelaryngeal node, can be involved in diffuse

squamous cell carcinoma of the head and neck or in isolation from laryngeal or thyroid carcinomas.2

Level VI nodes can also be involved in cervical esophageal cancers.

 Retropharyngeal nodes are a key area to evaluate with imaging, as this area is not included in a

typical neck dissection and cannot be assessed on physical examination. Tumor spread to

retropharyngeal nodes can result from nasal cavity or paranasal sinus primary, as well as from the soft

palate or pharynx (both the nasopharynx and oropharynx).2 Of these, primary tumors of the

nasopharynx are most closely associated with retropharyngeal nodes.

Virchow’s node is a left supraclavicular node typically described as being located near the

junction of the thoracic duct and the left subclavian vein where much of the body’s lymph drains into

the systemic circulation.14 It can be involved not only in head and neck cancers, but also in thoracic and

abdominal malignancy.14

Nodal Staging

Squamous Cell Carcinoma

Metastatic lymphadenopathy in the neck is most commonly from a primary squamous cell

carcinoma of the aerodigestive tract, less frequently from salivary gland malignancy, thyroid cancer,

nasopharyngeal carcinoma, or skin cancer. Staging allows clinicians to risk stratify patients therein

linking disease burden to prognosis and management strategies. The most commonly used staging

system for head and neck squamous cell carcinomas is the TNM classification developed by the

American Joint Commission on Cancer with the 8th edition published in 2016.25 As in all sites, the three

descriptors comprising the TNM classification for head and neck cancer include the primary tumor (T),

the extent of nodal involvement (N), and the presence or absence of distant metastases (M).25 The TNM

status is then tabulated to confer a stage of disease (i.e., Stage I, II, III, or IV).
Nodal staging for head and neck cancers was recently modified in the 8th edition of the AJCC TNM

classification scheme with several new categories added.25 Nodal metastasis with extranodal extension

markedly reduces 5-year survival in HPV-negative head and neck cancers.25–28 As such, this is now

incorporated into the guidelines, highlighting its prognostic importance. Although imaging is poor at

identifying small areas of extracapsular spread, the specificity is very high, which can be helpful in

therapy planning. Extranodal extension is defined by the AJCC manual as indistinct nodal margins,

irregular nodal capsular enhancement, or infiltration into the adjacent fat or muscle.25 Given the rise in

prevalence of high-risk human-papilloma-virus-mediated oropharyngeal cancers, and the management

and prognostic differences between HPV-mediated cancers and those related to tobacco and alcohol

use, the nodal staging for HPV-mediated cancers has been separated into its own category.25,26 HPV-

mediated cancers are defined as those demonstrating p16 overexpression.25 Immunohistochemistry for

p16 overexpression was chosen as a surrogate marker for high-risk HPV as its upregulation is seen in

cancers caused by HPV-16 and, though less commonly, HPV-18.25 HPV-negative oropharyngeal and

hypopharyngeal cancers share a nodal staging.25 Conglomerate nodal clusters are measured as a single

unit. Given the prognostic impact of extranodal extension, its incorporation into nodal staging has also

been modified from prior editions.25 The AJCC uses a similar level scheme to separate lymph node

groups by location as previously described.25 What follows is a discussion of the clinical N staging in head

and neck cancers. Pathologic N staging for patients who have undergone neck dissection is beyond the

scope of this chapter.

For HPV-negative oropharyngeal cancers in which no regional lymph node metastases are

evident, the category N0 is used (Table 1). A metastasis in a single lymph node, ipsilateral to the primary

site, measuring 3 cm or less in greatest dimension, and without extranodal extension is considered N1

disease. The N2 category is reserved for solitary ipsilateral metastatic lymph nodes measuring between

3 and 6 cm without extranodal extension (N2a), multiple ipsilateral lymph nodes none of which measure
more than 6 cm in greatest dimension and without extranodal extension (N2b), or metastasis in multiple

bilateral or contralateral nodes, none of which measure more than 6 cm in greatest dimension and

without extranodal extension (N2c). When lymph nodes measure greater than 6 cm without extranodal

extension, the N3a category is used. Metastasis in any node with extranodal extension is classified as

N3b. If the regional lymph node status cannot be assessed, the Nx category is used. It should be noted

that all N2 or N3 nodal categories confer stage IV disease. The N classification of lip and oral cancer,

major salivary gland cancer, nasal cavity and paranasal sinus cancer, and laryngeal cancer is identical to

that of HPV-negative oropharyngeal and hypopharyngeal cancer.

The presence of extranodal extension has not been shown to provide useful prognostic

information in HPV-mediated oropharyngeal cancers.25 As such, this is not included in the newly created

clinical nodal staging for HPV-mediated oropharyngeal cancers. The absence of regional nodal

metastases in HPV-mediated oropharyngeal cancers is described as N0 disease (Table 2). One or more

ipsilateral nodal metastases, none greater than 6 cm, fall into the N1 category. Contralateral or bilateral

nodal metastases, none greater than 6 cm, is described as N2. Nodes greater than 6 cm are described as

N3. While N3 (N3a or N3b) disease in HPV-negative cancers confers stage IV disease, clinical N3 disease

in HPV-mediated oropharyngeal cancers is stage III.25

An additional new category to the staging of head and neck cancers includes the finding of a

squamous cell carcinoma in lymph nodes arising from an undetected primary. If the primary cannot be

elucidated from history, exam, imaging, or biopsy of candidate sites, the pathologic node(s) should be

tested for the presence of Epstein-Barr virus (EBV), p16, and the direct presence of HPV by in situ

hybridization.25,26 EBV positive nodes are staged as nasopharyngeal carcinoma (see below). Nodes

positive for p16 and HPV in situ hybridization are staged as HPV-mediated oropharyngeal cancers.25,26
HPV-unrelated and EBV-unrelated occult primaries use the same clinical N stage as HPV-negative

oropharyngeal and hypopharyngeal cancers, however the final TNM stage differs.25

Nasopharyngeal Carcinoma

Squamous cell carcinoma arising in the nasopharynx uses a slightly modified TNM scheme (Table

3). Similar to cancers from other sites in the head and neck, N0 is used for nasopharyngeal cancers

(NPCs) in which no regional lymph node involvement is seen. Nodal metastases that occur in the midline

are defined as ipsilateral nodes. N1 is used for cases in which unilateral lymph node metastases are seen

measuring 6 cm or less in greatest dimension, and/or unilateral or bilateral retropharyngeal nodes

measuring 6 cm or less in greatest dimension, above the caudal border of the cricoid cartilage. N2 is

used for bilateral cervical nodal metastases measuring 6 cm or less in greatest dimension above the

caudal border of the cricoid cartilage. When nodal metastases measure more than 6 cm in greatest

dimension and/or are located in whole or in part below the caudal border of the cricoid cartilage, N3 is

used. Nx is again used when regional lymph node status cannot be or was not assessed.

Thyroid Carcinoma

Regional lymph node metastases are fairly common in thyroid cancer, but of less prognostic

impact in well-differentiated tumors (e.g., papillary or follicular) when compared to medullary thyroid

cancer (Table 4).25 The first echelon of nodal spread is to level VI nodes (paralaryngeal, paratracheal, or

Delphian nodes).25 Level IV and VII nodes can be secondarily involved. Bilateral nodal involvement is

common. As with squamous cell carcinoma, Nx is used when regional lymph node involvement cannot

be assessed and N0 is used when there is no regional lymph node involvement. When regional
metastatic lymph nodes are present, N1 is used. N1 can be further subdivided into N1a and N1b with

N1a including involvement of level VI or VII and N1b used for metastases to unilateral, bilateral, or

contralateral lateral neck lymph nodes (levels I, II, III, IV, or V) or retropharyngeal nodes. Staging is

usually separated by histologic type of thyroid carcinoma, as the expected 5-year mortality differs for

each.

Salivary Gland Tumors

Regional lymphatic spread from salivary gland primaries is less common when compared to

squamous cell carcinomas of the head and neck.25 Low-grade tumors rarely metastasize to regional

nodes, whereas the risk of nodal spread is substantially higher for high-grade tumors.25 Initial spread for

parotid tumors tends to be first to intraglandular or juxtaglandular nodes followed by level II or

retropharyngeal nodes.25 Bilateral nodal involvement is rare. The nodal classification for salivary gland

tumors is identical to that of HPV-negative squamous cell carcinomas of the head and neck.25

Summary

While head and neck anatomy is quite complex, it can be simplified using knowledge of major

landmarks to separate the neck into classically defined triangles. These landmarks are also useful for

defining the nodal anatomy of the neck. There are multiple systems for describing the nodal anatomy of

the neck, but this review focuses primarily on the system most commonly used by radiologists.21,22 In

this imaging-based classification, neck nodes are divided into discrete levels (I-VII) similar to the surgical

node classification.
 Distinguishing between normal-appearing nodes and pathologic nodes is of critical importance

in diagnosis, treatment, and prognosis in the patient with head and neck cancer, and will be further

discussed in chapter 2. Normal nodes are small and oval or reniform in shape with a fatty hilum, smooth

margins, and homogeneous internal characteristics with uniform enhancement post-contrast.

Head and neck cancers typically have a predictable pattern of spread along lymphatic drainage

pathways, which can help direct the radiologist, surgeon, or clinician to specific lymph node levels when

a primary head and neck cancer is identified. Knowledge of expected lymphatic drainage pathways can

also be of benefit in the patient presenting with nodal metastasis of unknown primary, to direct

attention to potential primary sites. Staging head and neck cancers is performed according to the AJCC

TNM Classification, recently updated to the 8th edition. Staging of squamous cell carcinomas of the

head and neck were divided in the most recent edition into HPV-mediated and HPV-negative cancers.

Additionally, clinical and imaging findings of extranodal extension are now fully incorporated into nodal

staging.

References

1. Rouvière H, Tobias MJ. Anatomy of the human lymphatic system. 1938.

2. Som PM, Curtin HD. Head and Neck Imaging. Elsevier Health Sciences; 2011.

3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin.
2011;61(2):69-90.

4. Chong V. Cervical lymphadenopathy: what radiologists need to know. Cancer Imaging.

2004;4(2):116-120.

5. Branstetter BF, Weissman JL. Normal anatomy of the neck with CT and MR imaging correlation.
Radiol Clin North Am. 2000.
http://www.sciencedirect.com/science/article/pii/S003383890570213X.

6. Rosse C, Gaddum-Rosse P. Hollinshead’s Textbook of Anatomy. Vol 741. Lippincott Williams &
Wilkins; 1997.
7. Weissman JL, Carrau RL. Anterior facial vein and submandibular gland together: predicting the
histology of submandibular masses with CT or MR imaging. Radiology. 1998;208(2):441-446.

8. Liu M-E, Barton F. Branstetter IV, Whetstone J, Escott EJ. Normal CT Appearance of the Distal
Thoracic Duct. American Journal of Roentgenology. 2006;187(6):1615-1620.

9. Standring S. Grays Anatomy 40thEdition. Anatomical Basis Of Clinical Practice, Churchill Livingstone,
London. 2008;40:415.

10. Escott EJ, Branstetter BF. It’s Not a Cervical Lymph Node, It’s a Vein: CT and MR Imaging Findings in
the Veins of the Head and Neck. Radiographics. 2006;26(5):1501-1515.

11. Kao J, Lavaf A, Teng MS, Huang D, Genden EM. Adjuvant radiotherapy and survival for patients with
node-positive head and neck cancer: an analysis by primary site and nodal stage. Int J Radiat Oncol
Biol Phys. 2008;71(2):362-370.

12. Castelijns JA, van den Brekel MWM. Imaging of lymphadenopathy in the neck. Eur Radiol.
2002;12(4):727-738.

13. Curtin HD, Ishwaran H, Mancuso AA, Dalley RW, Caudry DJ, McNeil BJ. Comparison of CT and MR
imaging in staging of neck metastases. Radiology. 1998;207(1):123-130.

14. Hoang JK, Vanka J, Ludwig BJ, Glastonbury CM. Evaluation of cervical lymph nodes in head and neck
cancer with CT and MRI: tips, traps, and a systematic approach. AJR Am J Roentgenol.
2013;200(1):W17-W25.

15. Som PM. Detection of metastasis in cervical lymph nodes: CT and MR criteria and differential
diagnosis. AJR Am J Roentgenol. 1992;158(5):961-969.

16. Gor DM, Langer JE, Loevner LA. Imaging of cervical lymph nodes in head and neck cancer: the
basics. Radiol Clin North Am. 2006;44(1):101-110, viii.

17. Kaji AV, Mohuchy T, Swartz JD. Imaging of cervical lymphadenopathy. Semin Ultrasound CT MR.
1997;18(3):220-249.

18. Rouviere H. Lymphatic system of the head and neck. Anatomy of the human lymphatic. 1938.

19. Shah JP, Strong E, Spiro RH, Vikram B. Surgical grand rounds. Neck dissection: current status and
future possibilities. Clin Bull. 1981;11(1):25-33.

20. Robbins KT, Clayman G, Levine PA. Neck dissection classification update: revisions proposed by the
American Head and Neck Society and the American Academy of Otolaryngology–Head and …. –
head & neck …. 2002.
http://archotol.jamanetwork.com/article.aspx?articleid=482968&resultclick=1.

21. Som PM, Curtin HD, Mancuso AA. An imaging-based classification for the cervical nodes designed as
an adjunct to recent clinically based nodal classifications. Arch Otolaryngol Head Neck Surg.
1999;125(4):388-396.
22. Som PM, Curtin HD, Mancuso AA. Imaging-based nodal classification for evaluation of neck
metastatic adenopathy. AJR Am J Roentgenol. 2000;174(3):837-844.

23. Deschler DG, Moore MG, Smith RV, eds. Quick Reference Guide to TNM Staging of Head and Neck
Cancer and Neck Dissection Classification. fourth. Alexandria, VA: American Academy of
Otolaryngology-Head and Neck Surgery Foundation; 2014.

24. Hermans R. Head and Neck Cancer Imaging. Springer Science & Business Media; 2012.

25. Amin MB, Edge SB, Greene FL, et al. AJCC Cancer Staging Manual. Springer International Publishing;
2016.

26. Lydiatt WM, Patel SG, O’Sullivan B, et al. Head and Neck cancers-major changes in the American
Joint Committee on cancer eighth edition cancer staging manual. CA Cancer J Clin. 2017;67(2):122-
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Figure Captions

Figure 1. Hyoid bone. Drawing of the segments of the hyoid bone, including the central body (B) and

greater cornua (GC). The lesser cornua (LC) project superiorly from the junction of the body and greater

cornua.

Figure 2. Laryngeal cartilages. The thyroid cartilage consists of two flat alae (a) which meet in the

midline to form the laryngeal prominence (LP). Superior cornua (SC) and inferior cornua (LC) project

from the posterolateral margins of the alae. The smaller, thicker cricoid cartilage consists of a full ring

comprising both an anterior arch (AA) and posterior arch (behind to the thyroid ala).

Figure 3. Neck muscles. The anterior (AD) and posterior (PD) bellies of the digastric muscle emerge from

a common central tendon similar to the superior (SO) and inferior (IO) bellies of the omohyoid muscle.

The sternocleidomastoid muscle (SCM) arises from the sternum and clavicle to insert upon the lateral
aspect of the mastoid process. The trapezius muscle (TM) extends from the occipital bone to span the

cervical and thoracic vertebrae and drape over the shoulders.

Figure 4. Relationship of the internal and external carotid arteries. Sagittal oblique CT reformat of the

right common carotid artery at the level of the bifurcation showing the relationship of the internal (Int)

to the external (Ext) carotid arteries.

Figure 5. Relationship of the anterior facial vein to the adjacent submandibular gland. Axial post-contrast

CT of the neck showing the normal relationship (A) of the anterior facial vein (arrow) draping over the

anterolateral aspect of the submandibular gland (broken arrow). In the comparison image (B), the

anterior facial vein (arrow) courses between a necrotic node (N) and the submandibular gland (broken

arrow) Masses arising from the submandibular gland will displace the anterior facial vein, while nodal

metastases will be separated from the submandibular gland by the vein.

Figure 6. Cervical triangles. The anterior triangle is divided into the submandibular (SMa) and submental

(SMe) triangles by the anterior belly of the digastric muscle. The carotid triangle can be subdivided into

superior (CS) and inferior (CI) triangles by the superior belly of the omohyoid muscle. The posterior

triangle can be subdivided into the occipital (OT) and supraclavicular (SC) triangles by the inferior belly

of the omohyoid muscle.

Figure 7. Normal lymph node appearance on imaging. Axial post-contrast CT (A) demonstrates normally-

configured right levels Ib and IIa lymph nodes with smooth margins, homogeneous enhancement,

reniform shape, and normal fatty hila. Similar normal configuration is seen on T1-weighted MRI (B) in

these right-sided neck nodes which are near-equal in signal intensity to muscle. On T2-weighted fat-

suppressed MRI (C), these bilateral level Ia and Ib nodes are hyperintense to muscle but maintain their

normal configuration.
Figure 8. Abnormal lymph node configuration and nodal necrosis. Coronal reformatted CT shows

multiple bilateral necrotic nodes (solid arrows) at multiple lymph node levels in a patient with

hypopharyngeal squamous cell carcinoma. Additional normal sized nodes with an abnormally rounded

configuration and obliteration of the central fatty hilum are also indicative of metastasis (broken

arrows).

Figure 9. Cervical node levels. Lymph nodes levels (I-VI) shadowed over a diagram of the lateral neck.

Level I can be subdivided into Ia and Ib by a line through the posterior edge of the submandibular gland

(SMG). Level II can be subdivided into IIa and IIb by the posterior edge of the internal jugular vein. Level

V can be subdivided into Va and Vb at the level of the lower margin of the cricoid cartilage. The medial

boundary of level III is the common or internal carotid artery.

Figure 10. Metastatic level Ib lymph node. Axial post-contrast CT showing a large right level Ib necrotic

lymph node in this patient with Merkel cell carcinoma of the lower lip.

Figure 11. Level II nodal metastasis. Necrotic right level II lymph node in a patient with metastatic

melanoma.

Figure 12. Retropharyngeal lymph node metastasis. Axial post-contrast CT (A) and fused axial PET/CT (B)

images of a patient with history of HPV-positive squamous cell carcinoma of the left faucial tonsil, now

status post left neck dissection and chemoradiation. There is an enhancing, FDG-avid left

retropharyngeal lymph node (arrows), indicating recurrence at a clinically-invisible site.

Figure 13. Boundaries separating levels IV, V, and VI in the lower neck. Axial post-contrast CT just above

the level of the thyroid gland was selected to clarify the boundaries of nodal stations in the lower neck.

Level VI includes nodes medial to the medial margin of the internal carotid artery on axial sections. Level

IV includes nodes between the medial margin of the internal carotid artery and an oblique line drawn
between the lateral margins of the sternocleidmostoid muscle (SCM) and anterior scalene muscle (ASc).

Level V nodes are lateral to this oblique line.

Figure 14. Metastatic Virchow’s node. Axial post-contrast CT demonstrates a necrotic left level IV node

(Virchow’s node, arrow) in this patient with known history of pancreatic cancer. Virchow’s node

receives metastases from abdominal or pelvic primaries without involvement of intervening thoracic

lymph nodes.

Figure 15. Metastatic Delphian node. FDG-PET/CT shows a markedly FDG-avid prelaryngeal (Delphian)

node in this patient with metastatic laryngeal cancer.

Figure 16. Named lymph nodes in the head and neck. Axial post-contrast CT images through the neck

demonstrate normal-appearing intraparotid (A), occipital (B), posterior auricular (C), and

retropharyngeal (D) lymph nodes.

Table 1.25 TNM Staging of Regional Lymph Nodes for HPV-Negative Head and Neck Cancers. *Extranodal

extension (ENE). Clinical and pathologic ENE should be recorded as ENE(-) or ENE(+). The designation of

“U” or “L” may be used for any N stage to indicate metastasis above (“U”) or below (“L”) the lower

border of the cricoid cartilage.

Table 2.25 TNM Staging of Regional Lymph Nodes for HPV-Mediated Head and Neck Cancers.

Table 3.25 TNM Staging of Regional Lymph Nodes for Nasopharyngeal Cancer.

Table 4.25 TNM Staging of Regional Lymph Nodes for Thyroid Cancer.
Key Points

● Despite its complex anatomy, a knowledge of the major landmarks in the neck is crucial for

identifying and classifying pathology. These landmarks include the bony, cartilaginous,

musculoskeletal, and vascular structures that clinicians classically have used to divide the neck

into triangles.

● By convention, the cervical lymph nodes are divided into 7 surgical levels. As the presence of

nodal metastases is the single greatest predictor for recurrence and eventual distant

metastases, awareness of the locoregional spread patterns can be useful to guide clinical and

radiologic assessment.

● The staging of head and neck cancers has recently been updated to address both the poor

prognosis in the presence of extracapsular extension of nodal disease, and the increased

prevalence of HPV-mediated oropharyngeal cancers. The presence of extracapsular extension in

HPV-negative head and neck cancers confers a poor prognosis and is stage IV disease. However,

extracapsular extension does not provide useful prognostic information in HPV-mediated head

and neck cancers, and is not used when clinically staging nodes from these tumors. While HPV-

mediated cancers have increased in prevalence, they are typically responsive to treatment, and

have a better overall prognosis.