StatePeter

of theM. Som,

ArtMD

Lymph

Nodes

of the

Neck

Index terms: Lymphatic system, CT, 276.1211 . Lymphatic system, diseases #{149} Lymphatic systern, flow dynamics #{149} Lymphatic system, MR studies, 276.1214 #{149} Lymphatic system, neoplasms, 276.375 #{149} Neck, neoplasms, 27.37 Radiology 1987; 165:593-600

ciated why? find and, one pose sues

with the worst prognosis and Finally (d), Can the radiologist the so-called occult primary tumor so, how often and where does concentrate such a search? The purof this article is to address these isand answer these questions.

racic duct In adults, and ded neck in fat.

or are

right lymphatic all lymph nodes entirely or in teleologically

duct (4). in the head part embedthis fat

Although

T

detailed and informed evaluation of the cervical lymph nodes may represent one of the most challenging problems that a radiologist faces today. The apparent difficulty of the task arises because many imagers are unfamiliar with the anatomy of the head and neck and thus are unsure where to initiate their search for these myriad nodes. Once a lymph node is identified, the radiologist must then determine the most accurate nomenclature to use in describing the findings to the clinician. Just as important, the radiologist must determine the criteria to be used in evaluating whether a node is pathologic and also the sensitivity of these criteria. The importance of clinical correlation and a sense of the impact that the radiologists findings have on the patients management are often lost in the pure mechanics of evaluating images. Several questions that address these issues should be asked during evaluation: (a) Can the radiologist identify clinically occult nodes and, if so, how often and what may this mean to patient prognosis and treatment? (b) What is the impact on patient survival of extranodal spread, and can it be accurately diagnosed on images? (c) Do diseased lymph nodes in all of the various anatomic locations of the neck have the same prognostic significance and, if not, which nodes are assoHE

HISTORICAL

PERSPECTIVE

Computed tomography (CT) as a diagnostic tool has been clinically available for just over a decade and has been used specifically to evaluate cervical lymph nodes only since 1981 (1). Before that time, the radiologist could offer little effective aid to the clinician evaluating disease of these nodes. The only pertinent radiographic examination was lymphangiography, and this procedure was associated failure, tremely with a high primarily small frequency due lymphatics in of technical exarea most to deep-lying, the

may provide a good medium for the smooth and easy motion of the muscles, vessels, and nerves, it also provides an outlining matrix for the cervical lymph nodes and allows CT and MR to depict these nodes well. Only two areas in the head and neck have no direct lymphatics: (a) The orbit virtually devoid of lymphatics and (b) muscles do not have lymphatics; rather,their lymph drains in the fascial planes

is

between vessels

muscles and around that supply them (4).

the

blood

ANATOMY NOMENCLATUREThe classification

AND

of cervical

lymph

nodesdifferent

is complicatedsystems and

by thethe

use of severalloose in-

commonly used for injection of contrast material: the retroauricular region (2). In addition, these studies were fraught with interpretive difficulties, primarily relating to the inability to distinguish malignant nodal from reactive nodal filling defects. Proximal metastatic nodal disease near the injection site could prevent visualization of distal lymph nodes. Finally, previous surgery, disease, or irradiation could alter or disrupt the usual lymphatic pathways, leading to either a nondiagnostic or a misleading lymphangiogram (2, 3). With the advent of CT, a noninvasive modality became available that allowed consistent identification of most pathologic cervical nodes, and it is not surprising that cervical lymphangiography has been virtually abandoned.

rather

termixing lar node5-12). nodes Of in and are system

of specific names for a particufrom one system to another (2,the the approximately body, about 300 800 lymph are of them

locatedfifth body

in theone-sixth located

neck.in

Thus,of all either

between

onethe

the nodes in side of the (4).

neck,tion

making

developmentvery complex

of a classificadi-

The cervical lymph nodes are often vided into four or five groups, all ofwhich Most are systems continuous are based with on each the other. work of

Rouviere sion. Any minology

(8), as is the following alternate, commonly will be pointed out.

discusused ter-

Rouviere

described

a lymphoid

collar

OVERVIEWIn the overall schematic of the lymphatic system, the lymphatic vessels commence as lymphatic capillaries in the soft tissues and extend as a closed system to larger vessels that pass into lymph nodes. The lymph then passes again in a closed network, usually to other nodes and then eventually to the neck veins via the thoracic duct. Thus all lymphatic flow filters through at least one node, and usually several nodes, before it reaches the tho-

of nodes, the pericervical ring, that encircles the neck at the junction of the head and neck. The nodes in this collar group include the occipital, mastoid, parotid, facial, retropharyngeal, submaxillary, sub-

mental,and ing lateral chains

and

sublingual

nodes.

Anterior

cervical groups are descendthat extend from this collar

From the Departments of Radiology (1234) and Otolaryngology, Mount Sinai Medical Center, City University of New York, One Gustave L. Levy P1., New York, NY 10029-6574. Received September 9, 1987; accepted September 14. Address reprint requests to the author. RSNA, 1987

down along the front and sides of the neck, respectively (Fig. 1) (8). The most clinically important lymph nodes in theconsideration of head and neck cancer are

the submaxillary, submental, yngeal, and lateral cervicalfollowing nodal groups. is a brief description

retrophargroups. Theof all the

593

1.

2.

Figures 1, 2. (1) Diagram of the neck in the left anterior oblique projection with a transverse slice made near the level of the floor of the mouth or junction of the head and neck. Component nodes from six cervical chains (occipital, mastoid, parotid, submaxillary, facial, and submental) form an outer collar of lymph nodes at this level; these palpable nodes are supplemented by the more centrally placed retropharyngeal and sublingual nodes. Descending from this collar are anterior and lateral cervical groups of nodes. (2) Diagram of the head and neck in the left anterior oblique projection demonstrates the palpable cervical node chains and their classic names. Any commonly used alternate names and the number of nodes in each chain are given in parentheses. The clinically important retropharyngeal nodes are not illustrated in this diagram.

The

occipital

nodes

junction

of the

upper

are situated posterior

at the portion

The

facial follow

nodes

are course and

situated

in the

sub-

of

cutaneouseral, maxillary

tissuesthe artery

of thethe

faceof the

and,external

in genfacial

the neck and the lower vault. There are three group, they drain the

lateral cranial to ten nodes in this occipital region and

upper lips, cheek, nose, anterior nasal fossae, most of the gums, teeth, palate, antenor portion of the tongue, medial portion

anterior

of the eyelids,gual glands,

submandibularand the floor

andof the

sublinmouth.

vein.group, mid

Therewhich portion

are fivedrains of the

to tenthe face and,

nodeseyelids, rarely,

in thischeek, the

directcessory The

flowchain mastoid

primarilyof the nodes

intolateral

the spinalcervical

acnodes.

Their lymph drains into the internal jugular chain of the lateral cervical nodes.Although these nodes almost may always clinically be distin-

lie just behind the ear. There are one to four nodes and they drain the parotid region, parietal area, and skin of the auricle, and their lymph flows into the inferior parotid nodes and superior internal jugular chain of the lateral cervical nodes. The nuchal izodes, which were not described by Rouviere, are a small separate group of one to three nodes that lie under the origin of the trapezius muscle tendon and extend downward and parallel to themidline. They typically become palpable

gums and palate. The into the submandibular The retropharyngeal

facial nodes drain nodes. nodes are separated

mimicgland,

a massthey can

in the submandibular MR.lie in the superficial submental to the

into

median

and

lateralnear the posterior

groups.midline to the

The

me-

dial group lies usually directly

and is upper

guished with CT and The submental nodestriangle of the neck,

in patients with infectious mononucleosis (13). The parotid nodes are situated both superficial to the gland and within the gland tissue. They are commonly referred to as either extraglandular or intraglandular and include seven to 19 nodes (12). These nodes may be confused both clinically and on CT and MR images with parotid sive gland and tumors. varied They territory drain including an extenthe

pharynx near the level of the second cervical vertebra. These nodes can, however, occur as low as the level of the greater cornua of the hyoid bone. There usually are only one or two nodes in this inconstant group. The lateral group, consisting of one to three nodes, is situated near the lateral aspect of the posterior pharyngeal wall, overlying the longus capitus and longus coli muscles. These nodes can extend along the entire length of the phar-

mylohyoid nor belliesare one

muscle of the

and between the antedigastric muscles. Therenodes in this group,

to eight

which

drains

the chin,floor Their

lowerof the lymph

lip,

cheeks,and into

anterior gingiva, tip of the tongue.

mouth, drains

forehead and temporal regions, portions of the mid and lateral parts of the face, the auricle and external auditory canal, the eustachian tube, portions of the posterior part of the cheek, buccal mucous membrane, gums, and the parotid gland itself. Overall the most common area to drain into these nodes is the skin, and thus the most common tumors to metastasize to them are melanomas and squamous cell carcinomas (3). The lymph from these nodes flows via a variety of local pathways to the internal jugular chain of the lateral cervical nodes.

ynx and are often enlarged in newborn infants with a pharyngeal infection. The lateral retropharyngeal nodes lie medial to the carotid artery, and this anatomic relationship may help distinguish such nodes from other retrostyloid parapharyngeal space masses. As a group, the retropharyngeal nodes primarily drain the nasopharynx and oropharynx; however, they also drain the palate, nasal fossae, paranasal sinuses, and middle ear.Their ternal nodes. lymph jugular drains chain into the superior inof the lateral cervical

The submandibular (submaxillary) nodes are situated in the submandibular triangle of the neck, lateral to the anterior belly of the digastric muscle and near thesubmandibular six nodes in this gland. group, There which are three drains to the

the submandibular nodes and internal jugular chain of the lateral cervical nodes. The sublingual nodes are inconsistent and lie in a lateral group along the anterior lingual vessels and in a medial group between the genioglossus muscles. They drain the tongue and floor of the mouth. They probably should not be strictly grouped as lymph nodes, but rather as small lymph nodules located along the collecting lymphatic trunks of the tongue and sublingual glands (12). Their lymph drains into the submandibular and submental nodes and the internal jugular chain of the lateral cervical nodes. The anterior cervical nodes lie in the infrahyoid portion of the neck, between the two carotid sheaths. There are two divisions of this group. The anterior (superficial) jugular chain follows the course of the anterior jugular vein and lies in the superficial fascia of the neck, overlying the strap muscles. These one to four small, inconstant nodes drain the skin and muscles of the anterior portion of theneck, and their lymph drains into the

lateral

portion

of the chin,

the

lower

and

594

#{149}

Radiology

December

1987

the

nodes

of Virchow

(Trosier

or

signal

nodes). They may receive metastatic implants from tumors originating in the abdominal and thoracic cavities (7). The terminations of these chains differslightly on each side. First, the respective

chains form jugular lymphatic trunks. On the right side this trunk enters either the right lymphatic duct, the subclavian vein,or the internal jugular vein. On the left

side the jugular lymphatic trunk terminates either in the arch of the thoracic duct or directly into the subclavian or internal jugular veins. Since these nodes lie outside the carotid sheath, the internal carotid artery,

commonjugular

carotidvein fat in should the

artery,

and

thebe

internalsharply space,

normally

outlinedby the

on CT and

MR scans,

silhouetted

nasopharyngeal

Figure

3.

Diagram

of the head

and

neck

in

and neck malignancies (4). They provide the major drainage for all of the other nodal chains. These nodes have been grouped according to location. The superf icial group contains one to four nodes andfollows the course of the external jugular

visceral space, and the posterior triangle. The spinal accessory (posterior triangle) chain of nodes follows the course of the spinal accessory nerve in the posterior tnangle of the neck. There are four to 20nodes in this group. The most superior

the left anterior oblique projection. The palpable nodes are indicated with use of a simplified nomenclature of roman numerals I-

VII (see Table

1). The clinically

important

retropharyngeal nodes are not included in this system and must be referred to separately. The internal jugular vein is lateral to the carotid artery (A) and parallels the course of the sternocleidomastoid muscle, while the

carotid artery neck. Becausethis vein

runs more vertically in the of this, under the skull base

to the artery, while in it lies anterior to the artery. The two bellies of the digastric muscle and the omohyoid muscle have also been drawn as reference points.

is posterior

the root

of the neck

thoracic duct or anterior mediastinal nodes on the left side and into the lowest internal jugular chain or highest intrathoracic node on the right side. The juxtavisceral chain of the anterior cervical nodes lies in relationship to the larynx, thyroid gland, and tracheoesophageal grooves. One of the pretracheal nodes, the Delphian node, lies on the cricothyroid membrane and receives lymph from the

vein, lying superficial to the sternocleidomastoid muscle. The deep group is divided into three subgroups: the internal jugular (deep cervical), the spinal accessory (posterior triangle), and the transverse cervical (supraclavicular) chains. The internal jugular (deep cervical) chain lies close to the internal jugular vein. Just under the skull base, these nodes become inseparable from the highest lymph nodes of the posterior triangle chain. Most of the 15 to 40 nodes in the deep cervical chain are concentrated below the level where the posterior belly of the digastric muscle crosses the vein and above the level where the omohyoid muscle traverses the system. This latter muscle divides the nodal chain into two clinically important groups: the superior (upper) or supraomohyoid nodes and the infraomohyoid

nodes blend with the highest nodes of the internal jugular chain, but while the internal jugular nodes descend almost vertically in the neck, the posterior tniangle nodes descend obliquely downward and postenolatenally in the neck. Thesenodes drain the occipital and mastoid

nodes, the panietal and occipital regions of the scalp, the nape, lateral portions of the neck, and the shoulder. Their lymphdrains tions primarily into the transverse cervichain.

cal chain,with

butthe

thereinternal

are alsojugular

communica-

The transverse cervical nodes follow the course

(supraclavicular) of the transverse

cervical vessels. The one to ten nodes in this group primarily connect the distal posterior triangle chain with the internal jugular chain and the central neck veins.

The

transverse

cervical

nodes

also

receive

subglottic larynx. Thus, when this node enlarged, subglottic disease is present. The juxtavisceral nodes have been subdivided into prelaryngeal, prethyroid, pretracheal, and laterotracheal groups. There are six to 16 nodes in this category,with most (two to nine nodes) in the tra-

is

(inferior) nodes. The superior group of nodes lies anterolateral to the vein, while the infraomohyoid nodes may be either anterior, medial, or posterior to the vein. The deep cervical nodes are arranged either in a single series or in two or three roughly parallel, interconnecting rows that are side by side. They drain the parotid, submandibular, submental, retropharyngeal, and some anterior cervical nodes. The nodes caudal to the level ofthe crossing of the omohyoid muscle also

lymph from the subclavicular skin of the anterolateral portion

nodes, the of the

neck, and the upper anterior chest wall. They drain in a manner similar to the internal jugular nodes. These complex relationships are summarized in Figure 2. Because of the varia-

tions in terminology, a simplified nomenclature was suggested in 1981 (14) (Fig. 3, Table 1). This clinicoanatomic scheme divides the clinically palpable cervical nodes into seven groups or levels, eachdesignated not classify by a roman numeral. the pathologically It does important

cheoesophageal grooves. The highest nodes in the tracheoesophageal grooves may lie directly behind the posterior thyroid lobes; when in this location, thesenodes MR may scans be with confused either on both CT nodule and or a thyroid

receive lymph from the arm and the superficial aspect of the thorax. A single node in the deep cervical chain, which isusually larger than the adjacent nodes, is

retropharyngeal

nodes,

which

are

not

parathyroid adenoma. This nodal chain drains the supraglottic and infraglottic larynx, pyriform sinuses, thyroid gland, trachea, and esophagus. Their lymphdrains in the same manner as that of the

situated near the junction of the posterior belly of the digastric muscle and the internal jugular vein; it is called the jugulodigastric, sentinel, or tonsillar node. It receives lymph from the tonsil, neighboring mucous membranes, and the submandibular nodes. Similarly, at the level where the omohyoid muscle crosses the internal jugular vein is the juguloomohyoid cent node, nodes. which is larger than It receives all of the the adjalymph

easily identified by the clinician. Using this system, the radiologist can specifically identify a particular node seen on a scan (e.g., a high, intermediate,

or lowalso be

levelreferred

III node).

Level

I nodes(submental)

can

to as medial

or lateral (submaxillary) allows a more precisethe radiographic retropharyngeal CT or MR scans,

in location. This correlation betweenfindings. identified be referred If on

and clinical nodes are they should

anterior ly. The primary

jugular

chain

described

previousup the in head

lateral cervical nodes make nodes of clinical interest

from the or nodes

tongue. Among the in the deep cervical

most chain

inferiare

to as such, being located at a specific tomic reference level as seen on the ages (i.e., C-i, C-2, etc.).

anaim-

Volume

165

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3

Radiology.

595

a.

b.

C.

d.

e.

f.

Figure 4. (a) Transverse spin-echo, proton density-weighted MR image of the upper portion of the neck demonstrates bilaterally enlarged occipital nodes (0) and multiple bilateral parotid nodes (P) in this patient with sarcoidosis. Repetition time (TR) = 1,800 msec, echo delay time (TE) = 27 msec, 0.5 T. (b) Axial CT scan reveals bilateral parotid nodes (P) and posterior triangle (spinal accessory) (level V) nodes (S) in this patient with sarcoidosis. (c) Axial CT scan reveals both a medial and lateral retropharyngeal node (R) on the right side of this patient with acquired immunodeficiency syndrome. (d) Axial CT scan reveals bilateral internal jugular chain nodes (I) (level II) in the jugulodigastric region of the neck. The right node measures i cm in diameter and must be considered normal (hyperplastic). The left node measures 1.75 cm in diameter and is pathologic in this patient with carcinoma of the supraglottic larynx. SM = submandibular gland. (e) Axial CT scan reveals two left submandibular nodes (sni) (level I) in this patient with lymphoma. SM = submandibular gland. (f) Axial CT scan reveals bilateral lower-neck posterior triangle (spinal accessory) nodes (5) (level V) in this patient with lymphoma.

Since poorly logically used cervical

normal

lymph

nodes

are

often

seen on scans, if seen at all, pathoenlarged lymph nodes will be to illustrate nodes just some of the important (Fig. 4). discussed

the entire neck ternal auditorytop of the

from canal

the level of the ex(skull base) to the

can be given initially trated drip administeredThis latter technique

andallows

the concenthereafter.scanning

manubrium.

CT is performed with the patients chin slightly elevated. A gantry angle of 00 is used, and 5-mm-thick contiguous scans be are obtained after throughout the

IMAGINGThere are at least

PROTOCOLtwo approaches to

areashould

of interest.obtained

If possible,

the

scans

to be started immediately, with no time lost during contrast material administration. Magnetic resonance (MR) imaging protocols are more varied, dependingin unit part on being the used. magnet In nodes. 5 mm strength general, and transverse the

administration

imaging the neck: With one, only the area suspected of being pathologic is imaged, while with the other, the entire neck is imaged. The former approach provides short examinationtimes. However, in patients with ma-

of contrast material because these images will help in the differentiation between vessels and nodes and, in somecases, tissues. administered between The pathologic contrast as a drip material of 150 and normal is usually mL of a

imagescervical nesses

are

most

useful

forSection are

depictingthicksince optimal,

lymph of about

lignancy outsideIn addition, metastasize tween

there of theto the skull

may be occult disease clinically localized area.most the base primary neck and efficacious are the tumors located root of that bethe

concentrated iodinated agent (e.g., Conray [Mallinckrodt, St. Louis] 600 mg/mL); scanning is initiated when one-third of the bottle (50 mL) hasbeen 50 mL given. of Alternately, contrast material a bolus (e.g., of Hy25-

thicker sections may obscure small nodes. Because of time constraints, only the area of interest is usually imaged; however, with newer, faster imaging techniques and new software, thesetime limitations may become less of a

neck.lignancy

Therefore,it is more

in patients

withto

mascan

paque

50 [Winthrop-Breon,

New

York])

factor. Ti-weighted images usually good differentiation between

provide the inter-

596.

Radiology

December

1987

5.Figures 5, 6. (5) Axial CT scan reveals two necrotic

6.nodes in the right side of the neck. One

region of the internal jugular chain (I) (level II), and one is in the posterior triangle (5) (level V) of this patient with carcinoma. Both nodes are enlarged and have necrotic regions with irregular, nodular walls. (6) Axial CT scan reveals a necrotic, smooth-walled cystic mass in the right posterior triangle (level V) in this patient with metastatic papillary thyroid carcinoma. This is too far posterior in the neck to be a branchial cleftcyst of this size.

is in the jugulodigastric

mediate-signal-intensity lymph nodes and the high-signal-intensity fat. A similar, although less clear, distinction can be seen on proton density-weighted (mixed) images. On strongly T2weighted images, the pathologic nodes tend to become bright in intensity, whereas the surrounding fat now has an intermediate-intensity signal. On the T2-weighted studies, focal areas of high signal intensity may be seen in nodes, and these may represent sites oftumor necrosis.

The quality of the image depends most on the signal-to-noise ratio, which in turn depends on the surface coil used. At present, a variety of coils are being used by different manufacturers and individuals, and no one technique has been determined to be better than the others. Pathologically correlated studies must be done before optimal imaging sequences and coil designs can be determined.

CRITERIA FOR CERVICALOnce knowledge ture and the locationslymph tained, velop nodes the criteria next for on

EVALUATING NODESabout nomenclaof cervicalhas been step when obis to dea node

images important deciding

is pathologic. The nodes in the upper portion of the neck tend to be larger than those the lower portion; this is especially true of the submandibular and upper supraomohyoid nodes of the internal jugular chain (8, 12, 15). These nodes

in

become enlarged due to a benign reactive hyperplasia that is in response to the common inflammatory episodes that so often involve the teeth, gums, tonsils, and pharynx. Results of several clinical series with pathologic correlation have suggested that a clinically positive (metastatic) node should be defined as being greater than 1 cm in diameter, spherical rather than flat or ovoid, and harder than an uninvolved node (4, 16, 17). Other authors have indicated that, especially for the submandibular and internal jugular chain nodes, normal nodes are usually 1.5 cm in diameter or less; nodes in the other cervical chains are normally smaller than 1 cm in diameter (12, 15, 18, 19). It should be noted that most cervical lymph nodes are ovoid or lima bean shaped, and the determination of nodal size is based on the greatest nodal diameter. Thus, to correlate imaging findings with these clinical studies, contiguous images may have to be examined in some patients in order to determine accurately the greatest diameter of a node whose longest dimension is parallel to the craniocaudal axis. The smallest-sized nodes detected with palpation were approximately 0.5 cm for superficial nodes and 1 cm for deeper nodes (17). On the basis of these studies, the most reasonable size criteria to use when evaluating cervical lymph nodes in the submandibular (level 1) and jugulodigastric regions of the internal jugular chain (low level II, high level III) are that any node in these regions larger than 1.5 cm in diameter must be

considered abnormal, while for the remaining nodes in the neck a diameter of more than 1 cm should be considered abnormal (17, 20). On the basis of these criteria, about 80% of enlarged nodes are truly metastatic and 20% are enlarged due to benign hyperplasia; these statistics are similar to those reported by clinicians (17, 21, 22). The larger the size by which a node is considered abnormal, the fewer false-positive findings will be reported; however, as the number of false-positive findings decreases, the number of false-negative findings will increase. Because of this, in large cancer centers where the patient population is biased toward cancer, the smaller 1-cm-diameter criterion is often used for all nodes, to raise the diagnostic level of suspicion. This is usually done with the proviso that before such a borderline lymph node is called metastatic, it must be spherical rather than ovoid. It is known that cancer cells initially enter the lymph node via the afferent lymphatics and lodge in the reticular meshwork of the marginal sinuses of the nodal cortex. Proliferation of the malignant cells then results in invasion of the nodal medulla, extensive neoplastic invasion, blockage of the flow of lymph, and propagation of cancer cells to other nodal chains. Eventually the nodal medulla undergoes necrosis. Although this may occur within a brief period of time, metastatic nodal necrosis is a biologically late event in the evolution of the tumor in the lymph node (4, 23). Both CT and MR imaging can be used to detect nodal necrosis, even in nonenlarged nodes. This further increases the sensitivity of the overall nodal evaluation, for now both necrosis and nodal size are used as criteria.

Any node with central necrosis, regardless of size, must be considered pathologic. At CT, this necrosis usually appears as a central area of low attenuation (10-18 HU) with a surrounding irregular, nodular wall (1, 18) (Fig. 5). The nodal wall can, however, be smooth or uniform, simulating a benign process. This latter appearance ismost often associated with metastatic

papillary thyroid carcinoma rather than with squamous cell carcinoma (Fig. 6). Fatty nodal replacement can occur in postinflammatory and postirradiation nodes (18). This replacement usually occurs in a peripheral or noncentral location within the node. Although any measurement of the attenuation of such a small area is fraught with volume averaging errors, these regions usually measure near 0 HU andthus are at a lower attenuation than

metastatic necrosis Although there relevant correlation

(18). is little statistically between patholog-

Volume

165

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#{149} 597

a.

b.

C.

Figure 7. (a) Axial contrast material-enhanced CT scan reveals two adjacent necrotic nodes in the right jugulodigastric region of the internal jugular chain (level II). The nodes have enhancing, unsharp rims that suggest extracapsular invasion in this patient with pharyngeal carcinoma. (b) Spin-echo, proton density-weighted MR image of the neck near the same level as a reveals the enlarged right nodal mass. However, it is not evident that there are two conglomerate nodes rather than one large node. TR = 2,000 msec, TE = 30 msec, 0.5 1. (C) Spin-echo 12-weighted MR image, paired with b (TR = 2,000 msec, TE = 80 msec), reveals high signal intensity in the right nodal mass, suggesting necrosis. The capsular margins are also unsharp, suggesting extracapsular invasion.

ic and MR findings at this time, there initial evidence to suggest that areas high T2 signal intensity within alymph node may correspond to sites

is ofof

tumor necrosis, and that MR imaging may become a sensitive technique for the evaluation of these metastatic nodes (Fig. 7). In all patients presenting with cervical adenopathy, there is the possibility that a node, whether cavitated or not, will be inflammatory in origin. In mostbut guish not all between instances, history and physi-

cal examination andious

canan the

be used node.

to distinAn insida non-

inflammatory-related

a metastatichistory,

lymphabsence

of pain,

tender mass, and fixation all indicate a malignant lesion. Even so, there will be a few cases in which both the clinician and the radiologist cannot distinguish between the two possibilities; in these cases, only the pathologist can resolve the issue. Some further CT findings that can aid the radiologist in distinguishingbenign from malignant disease include

(a) the presence of a thick, irregular zone of enhancement around a necroticcentral matory area, process which indicates or an abscessed inflam(abscess

node-especially tuberculosis-or an infected branchial cleft cyst); (b) the presence of a thin, enhancing rim with one or more focal areas of nodularity(3, 24), which node indicates with capsular a malignant invasion; lymph

(c) the whichcess,

presence indicatessince most

of an enhancing an inflammatorytumor nodes have

node, proan

attenuation equal to or less than that of muscle; (d) the presence of nodes some of which enhance, some of which are of muscle density, and some of which are of a lower attenuation than muscle. These varied attenuations suggest agranulomatous process (Fig. 8).

Calcifications within cervical lymph nodes are unusual. Most often these calcific deposits are found with old granulomatous disease (scrofula). Metastatic tumoral calcifications are uncommon, and the most likely primary neoplasm is papillary thyroid carcinoma (Fig. 9). Healed, irradiated metastatic carcinomatous and lymphomatous nodes may in rare cases calcify. In addition, from a clinical and pathological perspective, about 5% of metastatic nodes will be clinically occult but will be detected by CT (18). These nodes lie primarily deep to the sternocleidomastoid muscle or in areas that are not accessible at routine examination, such as the retropharyngeal or tracheoesophageal regions. Thus, imaging techniques make the staging of metastatic nodes more accurate than if clinical examination is used alone. The advantage of imaging over palpation is also demonstrated when an obvious conglomerate mass of nodes seen on images is erroneously interpreted by the clinician as a solitary node. This distinction can influence the staging of the cervical nodes if the clinician believes that such a mass is less than 3 cm in diameter (25). The occurrence of extranodal tumor extension is an ominous prognostic sign and is associated with about a 50% decreased survival compared with the survival in patients with tumor confined to the lymph nodes (26). Although it used to be assumed that lymph nodes determined at physical examination to be smaller than 3 cm in diameter did not have extracapsular spread, it is known today that such extranodal tumor extension occurs in 23% of nodes smaller than 1 cm, 53% of nodes 2-3 cm, and 74% of nodes greater than 3 cm. Overall, extranodal spread occurs in 60% of nodes less than 3 cm in

Figure

8.

Axial

contrast-enhanced

CT scan

reveals multiple posterior triangle (level V) and internal jugular chain (level III) nodes in the left side of the neck. Some of these nodes enhance more than do the adjacent muscles, one or two are about the same at-

tenuation, and one or two have areas of lower attenuation. There is also a small, enhancing right internal jugular chain node (level III) (arrow) in this patient with tuberculosis.

diameter (26, 27). On CT images, extranodal spread is correlated with an unsharp or poorly defined nodal border that may or may not enhance. There also may be associated obliteration of the adjacent fat planes (1, 3). These findings are more indicative of metastatic disease if there is no history of prior surgery, irradiation, or recent infection, all of which can cause similar imaging findings (28).

598

#{149}

Radiology

December

1987

extracapsular spread, of nodal immunoreactivity, of the precise tumor site, and of the histologic characteristics of the tumor (32). These systems are currently based on clinical findings. However, there is hope that imaging will soon be a necessary part of this staging. If scanning is

used to complement clinical examination, the following staging conversions can occur: NO will become Ni neck, Ni will become N2 neck, Ni will becomeN3c neck, or NO will become N3c neck.

of patients with head and neck cancer, it was found that the number of deaths increased from distant metastases, decreased from uncontrolled tumor, decreased from fatal complications of treatment, and increased from unrelated nonmalignant disease. The frequency of a second malignancy as a cause of death remained constant at 14% (36).Thus, it appears we are seeing a change

Clearly, imaging state-of-the-art

is necessary to the evaluation of cancer.

CLINICALThe presence node in a patient tive tract cancer Invasioninous

PERSPECTIVEof a metastatic with upper is an ominousof the

cervical aerodigesproglocation

in the evolution of head and neck cancers, with distant metastases starting to become a serious treatment consideration; it is clear that the frequency of such distant metastases is greater in patients with metastatic disease of the cervical nodes (26). The location of a metastatic node in the neck, regardless of the site of theprimary tumor, may have a certain

of the

carotidAlthough

arteryin

hasmost

omsur-

nostic

sign.

Regardless

implications.

of thesingle

primarymetastatic

tumor,node

thein

presencethe ipsilateral

of a

casesrounding

effacementthe artery

of the

fat planesarterial

signifies

portionsurvival

of thein half.

neck

cuts

the

expectedaffect-

invasion, this is not always true (1, 28). Ultrasound has been employed to define better the true cases of carotid artery invasion, and although use of this technique can reduce the number of false-positive diagnoses made on thebasis still ologist of a few (29). CT imaging cases In that general, alone, will there defy a cautious the are radira-

A contralateral

diologic diagnosis of probable arterial invasion will usually be correct and will not effectively influence the treatment planning for these patients, whousually have more advanced disease.

ed node also reduces the expected survival by 50%. Thus, a patient with bilateral cervical metastases has only one quarter the expected survival he or she would have had if there were no metastatic nodes (33-35). The presence of extranodal tumor spread is the best prognosticator of local treatment failure and is also associated with a 50% decreased survival (3335).

At present, it is not possible to identify microscopic tumor implants in a normal-sized noncavitated node by means of any imaging technique. Similarly, although an educated guess can often be made about the nature of a pathologic area in an abnormal node based on its imaging appearance, no steadfast rules exist and histologic findings sometimes prove any of theserules to be in error.

Once the lymph nodes become obstructed, there may no longer be an orderly progression of disease down the lymphatic chains into the vascular system. Tumor cells may bypass the obstructed ginal medulla sinuses, or by they means may of enter the marthe

prognostic value. As an example, the mere presence of a metastatic level V node suggests a 19% worse 5-year survival compared with survival in patients who have metastatic nodes in any site other than the posterior triangle. Similarly, metastatic level IV nodes have an associated grave prognosis because most of them are metastases from a primary tumor located below the clavicle. About 2.8% of intrathoracic and intraabdominal malignancies will spread to these nodes (7). Similarly, if a primary tumor of the head and neck spreads to level IV nodes, more proximal nodes are probably already involved, and the patient has either a biologically aggressive tumor or a faradvanced malignancy. The preferred sites of metastasis for the various primary tumors of the head and neck have been thoroughly studied (3, 16). Although most of the neoplasms metastasize to level II and III

blood stream within the node. This phenomenon appears to account for the skip-type metastases that occur in some patients. On the other hand, lymphatic-venous shunting has been found in patients with nonobstructedlymphatics, and account metastases and argues this for against intercommunicathe confused in the some concept patpafound tion tern tients may of

CANCER

STAGING

SYSTEMS

nodes, some conclusions can be drawn from these analyses (Table 3). Tumors that have the highest frequency of metastasizing at clinical presentation, the highest frequency of bilateral nodal involvement, and the highest frequencies of posterior triangle adenopathy all arise from Waldeyer ring and, in particular, the nasopharynx (23). Since thisregion can be examined in physician detail when

There are two major TNM (tumor, node, metastases) classifications currently in use for the staging of head and neck cancers. The one more generally accepted in the United States was developed by the American Joint Committee on Cancer (AJCC). The other system was developed by the International Union Against Cancer (UICC). Although both systems correlate well with one another, the AJCC system may be more discriminative for nodal disease (Table 2) (30, 31). At present,however, cized nodal for both not location systems addressing in reference have the been issues both to critiof the

that metastases are strictly confined to one or another system (except, perhaps, early in the evolution of the disease (26). In recent years, there has been better control of local and regional cancer, and while patients are living somewhat longer, they are exhibiting the development of distant metastases. This may, in fact, only be the unmasking of thenatural history of head and neck cancer

thegist

entiremay be

neckthe

is imaged,first

the

radioloto local-

primary portions

tumor and to the of chains within

chains or the neck, of

with successfully treated local and regional disease, and it may be more correct to view head and neck cancer as a systemic disease rather than as a localregional process, as it has been traditionally viewed (26). In a recent study

ize the primary tumor in a patient presenting clinically with cervical metastases. This is especially true in the 4.7% of patients who present with an occult primary tumor and in whom imaging enables identification of as many as 25% of these clinically undiagnosed tumors (3, 20, 23, 37, 38). In addition, it is generally believed that when metastases are found at nodal levels not expected of a particular primary tumor, this neoplasm is more biologically aggressive than normal (16, 26). Thus, the radiologist shouldbecome familiar with the statistically

Volume

165

Number

3

Radiology

#{149} 599

expected nodal metastases for each of the primary tumors of the head and neck. Evidence suggests performance of an open biopsy on a neck node will decrease the patients survival unless definitive surgery is performed without delay (26). This has prompted the increased use of the skinny-needle biopsy procedure, with or without imaging guidance (38-40). In fact, new needle materials are being developed that reduce imaging artifacts and make imaging-guided biopsies more practical (41). A limiting factor in this procedure is lack of access to an expert cytologist; however, this problem appears to be diminishing, since interest in this technique has grown. Today, physicians at most institutions will perform a skinny-needle biopsy before surgically violating a neck for a diagnostic procedure. Even newer approaches are being investigated in which, by the use of thinneedle monitors, in vivo oxygen tension is being monitored to help the clinician evaluate the presence of tumor or the effectiveness of therapy (42). New techniques will continue to evolve in the quest to solve the problems of head and neck cancer.

Table Nodal

3

Metastases

in Patients

with

Head

and Neck

CancerPercentage of Percentage ofPatients Initially Who Present Patients with Bilateral Metastatic Nodes

Site

of Primary

Nodal

Levels

Most

Carcinoma Oral portion of tongue Floor of mouthRetromolar trigone

Commonly I, II, IIII, II

Involved

with

Metastases34-65 30-59 39-56

11.8 7.8 8.8 253L8 20.2

anterior fascial Soft palateNasopharynx

pillar

1, II, III II II, Ill, IV,II, 111, I, II, III, IV, II, III, IV,

37-56V V V V (22.3%) (10.9%) (9.0%) (8.4%) 86-90 50-71

Oropharynx Tonsillar

fossa

58-7652-72

139

Hypopharyn.x Base of tongue Supraglottic larynxNote-Data in table obtained

II, III, IV, II, Ill, IVfrom references

V (6.7%)

50-8331-54

21.322.5

17, 18, and

24.

7.

8.

Hollingshead WH. Anatomy for surgeons. 1, The head and neck. New York: Hoeber-Harper, 1954; 488-494. Rouviere H. Lymphatic system of the head

Vol.

26.

Collins

SL.

Controversies

in management

of

and

cancer of the neck. In: Thawley eds. Comprehensive management neck tumors. Vol. 2. Philadelphia:27. 1987; Snow 1386-1443. GB, Annyas AA, Van Slooten

SE, Panje WR, of head and Saunders,EA, Bartelink

neck.tern.

In: AnatomyTobias MJ

of the(trans.).

humanAnn Arbor,

lymphaticMich.:

sysEd-

9.

wards Brothers, 1938; 5-28. Last RJ. Anatomy regional

H, Hart and applied. 6th ed.28.

AA.

Prognostic

factors

of neck7:185-192. tomography

node

meof

10

11.

12.

Edinburgh: Churchill-Livingstone, 1978; 376378, 443-444. Montgomery WW. Surgery of the upper respiratory system. Philadelphia: Lea & Febiger, 1971; 75-87. Trotter HA. The surgical anatomy of the lymphatics of the head and neck. Ann Otol Rhinol Laryngol 1930; 39384-397. Feind CR. The head and neck In: Haagensen

tastasis. Clin Otolaryngol 1982; Som PM, Biller HF. Computed

the neck in the neck dissectionology 1983;

postoperative patient: and the myocutaneous

radical flap.

Radi-

148:157-160.

29.

Hajek PC, Salomonowitz E, Turk R, Tscholarkoff D, Kumpan W, Czembirek H. Lymph nodes of the neck: evaluation with US. Radiology 1986; I 58:739-742.Black RJ, Gluckman JL, Shumrick DA. Staging

30.

CD, Feind CR, Herter FP, Slanetz CA, Weinberg JA. eds. The lymphatics in cancer. Philadelphia: Saunders, 1972; 60-208.13. Kuisk of the H. Development. lymphatic system. structure, In: Kuisk and function H, ed. Tech-

systems

for cancerbetween 8:305-312. node

of theAJC

headand

andUICC.

neckClin

region:Otolar-

comparison yngol 1983;

CONCLUSIONClearly, imaging today plays an essential role in the evaluation of disease in the cervical lymph nodes and should be part of any thorough workup of patients with head and neck cancer. With the continued advance of techniques and the growing interest in head and neck imaging, it is only reasonable to expect that, in the future, imaging will have an even greater impact on patient management. #{149} Acknowledgments:I thank Hugh D. Curtin, M.D., William P. Dillon, M.D., and R. Thomas Bergeron, M.D., for their advice and editorialcomments script. in helping me prepare this manu-

31.

Johnsvical

ME, Neallymph

DA, Cantrellmetastasis:

RN. LaryngolPatel MF,

Staging 1984;Harvey

of cerof two

comparison

niquepretation.

of lymphographySt. Louis: neck Green,

and RH,

principles1971; 5-14.

of interB. Surgical32.

systems.332. Rapidis

AnnAD,

OtolLangdon

RhinolJD,

93:330PW.

14.

Shah

JP, Strong

E, Spiro

Vikram

15.

grand rounds, futurepossibilities Mancuso AA,

dissection: current status and Clin Bull 1981; 11:25-33. Harnsberger HR. Muraki AS. Ste-

vens MH. Computed and retropharyngeal

tomography lymph nodes

of cervical normal anatoin staganatomy. Ra-

33.

16.

my. variants of normal, and application ing head and neck cancer. I. Normal diology 1983; 148:709-714. Lindberg R. Distribution ofcervical

34.lymph node 35.

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squamous cell carcinoma of the and digestive tracts. Cancer

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18.

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1987