Está en la página 1de 21

C e r v i c a l Lym p h N o d e E v a l u a t i o n

and Diagnosis
Thomas C. Bryson, MD, Gaurang V. Shah, MD*,
Ashok Srinivasan, MBBS, MD, Suresh K. Mukherji,

MD

KEYWORDS
 Lymphadenopathy  Lymph node  Head and neck cancer  CT  MRI
KEY POINTS
 In many cases of cervical lymphadenopathy, the clinical history, physical examination,
and routine laboratory investigations can establish a presumptive diagnosis of reactively
enlarged nodes related to viral or bacterial infection. Imaging these patients is generally
unnecessary, unless atypical symptoms or findings concerning for aggressive infection
are noted.
 Imaging, particularly computed tomography (CT), is valuable in cases concerning for
suppurative lymphadenitis or deep neck infection by identifying abscesses requiring
surgical drainage.
 Imaging findings such as stranding of adjacent fat on CT may help distinguish suppurative
nodes from metastatic disease; however, common imaging findings such as nodal
enlargement, enhancement, and hypodensity seen in the setting of lymphadenitis caused
by typical or atypical pathogens can also be seen with nodal metastasis.
 In asymptomatic patients and patients with nonspecific symptoms, imaging may be indicated to assist in evaluating a palpable neck mass.

INTRODUCTION

Cervical lymphadenopathy is a common clinical finding, which can be related to reactive nodal hypertrophy, granulomatous processes, lymphoma and head and neck
cancers or mimicked by nonnodal neck masses. Cross-sectional imaging has the ability
to quickly assess the extent of cervical lymphadenopathy with greater accuracy than
the physical examination and provide information regarding the relationship with

Dr Mukherji is a consultant with Phillips Medical Systems. The other authors have nothing to
disclose.
Department of Radiology, University of Michigan Hospital and Health Systems, 1500 East
Medical Center Drive, Ann Arbor, MI 48109-5030, USA
* Corresponding author. Department of Radiology UH-B2-A209, University of Michigan Health
Systems, 1500 East Medical Center Drive, Ann Arbor, MI 48109-5030, USA.
E-mail address: gvshah@med.umich.edu
Otolaryngol Clin N Am 45 (2012) 13631383
http://dx.doi.org/10.1016/j.otc.2012.08.007
0030-6665/12/$ see front matter 2012 Elsevier Inc. All rights reserved.

oto.theclinics.com

1364

Bryson et al

adjacent vital structures. This information can have significant management implications in cases of acute infection, but is perhaps most important when applied to staging
of head and neck malignancies. Head and neck squamous cell carcinomas (HNSCC)
are the most common malignancy of the upper aerodigestive tract, and lymphatic
spread is the most important mechanism of metastasis in these patients. Accurately
staging nodal disease in HNSCC has both important prognostic and management
implications. This article discusses the rationale for imaging cervical lymph nodes
and reviews nodal anatomy and common drainage patters, imaging features of pathologic lymph nodes, and the advantages of various imaging modalities available.
RATIONALE FOR IMAGING

In many cases of cervical lymphadenopathy, the clinical history, physical examination,


and routine laboratory investigations can establish a presumptive diagnosis of reactively enlarged nodes related to viral or bacterial infection. Imaging these patients is
generally unnecessary, unless atypical symptoms or findings concerning for aggressive infection are noted. Imaging, particularly computed tomography (CT), has proved
valuable in cases concerning for suppurative lymphadenitis or deep neck infection by
identifying abscesses requiring surgical drainage.1,2 Imaging findings such as stranding of adjacent fat on CT may help distinguish suppurative nodes from metastatic
disease; however, common imaging findings such as nodal enlargement, enhancement, and hypodensity seen in the setting of lymphadenitis caused by typical or atypical (eg, mycobacterial or bacillary) pathogens can also be seen with nodal metastasis
(Fig. 1).3
In asymptomatic patients and patients with nonspecific symptoms, imaging may be
indicated to assist in evaluating a palpable neck mass. In the case of a solitary

Fig. 1. Contrast-enhanced CT shows a conglomerate of enlarged, heterogeneously


enhancing right level I and II lymph nodes (arrow) in an immunosuppressed patient with
fungal lymphadenitis. Note the adjacent inflammatory stranding and thickening of the
platysma muscle (arrowheads).

Cervical Lymph Node Evaluation and Diagnosis

palpable neck mass, imaging with ultrasonography (US), CT, or magnetic resonance
imaging (MRI) may identify congenital cysts such as thyroglossal and branchial cleft
cysts. Imaging findings in many of these patients are nonspecific, and recent studies
have questioned the ability of US to make a confident preoperative diagnosis.4
However, imaging in these types of patients should be able to differentiate between
nodal disease and nonnodal neoplasms in most cases. Nonnodal findings on imaging
can also affect the differential diagnosis. For example, multiple cystic lesions within
the parotid glands seen in combination with cervical lymphadenopathy can suggest
the diagnosis of human immunodeficiency virus infection.
The prognostic value of accurate staging in the case of head and neck malignancies
has produced a well-defined role for the use of imaging. Squamous cell carcinomas
(SCC), which make up 80% to 90% of all upper aerodigestive tract malignancies,
have shown a high predilection for metastasis to regional lymph nodes, with nodal
metastases present in 20% to 30% of patients at the time of diagnosis depending
on the site.5,6 The presence or absence of lymph node metastasis in these patients
at the time of diagnosis has a profound impact on 5-year disease-specific survival
rates. In 1 series evaluating HNSCC from multiple sites, the 5-year survival was
reduced from 67.9% to 39.9% based solely on the presence of nodal metastases.
Nodal stage in this series also affected survival, with advanced N2 or N3 patients,
according to the American Joint Committee on Cancer (AJCC) staging system,7
showing significantly worse outcomes.8 Staging examinations by palpation alone
have shown limited sensitivity of approximately 64%, specificity of 85%, and overall
accuracy of approximately 75%.9 Also, clinical examination has proved inaccurate
at evaluating size of cervical nodes regardless of clinical experience.10 The ability of
imaging studies to evaluate nodal groups occult to palpation (such as retropharyngeal
nodes) and provide accurate nodal measurements can increase sensitivity and specificity up to 81% and 96%, respectively,9 with imaging identifying palpably occult
nodal metastases in up to 27% of patients.11
Patients who are deemed N0 by clinical staging typically undergo elective treatment
of cervical lymph nodes such as neck dissection if there is a 20% risk of occult metastases.12 Imaging studies may increase sensitivity and specificity over palpation;
however, identification of micrometastases (metastatic deposits less than 3 mm in
size) remains a significant challenge for imaging. Up to 25% of neck dissection specimens may harbor only micrometastases13 and use of highly sensitive molecular
pathology techniques can show evidence for micrometastases in even more cases
than traditional light microscopy.14,15 Treatment of these N0 patients remains controversial, and some investigators have suggested that the rate of occult metastases in
patients undergoing thorough staging examinations including CT or MRI is low
(less than 10%), making observation a viable option with equivalent outcomes to elective neck dissection.8 Other investigators have advocated reducing the number of
staging evaluations used in patients with small primary tumors16; however, they
continue to advocate the use of cross-sectional imaging as an accurate and expedient
way to evaluate both the primary tumor and potential nodal metastases.
NODAL CLASSIFICATION

The complex anatomy of cervical lymph nodes has led to numerous attempts at organization. The most widely used schemes historically have been those, such as that of
Rouvie`re,17 describing nodal groups based on proximity to adjacent structures. This
type of organization resulted in the familiar large groupings of cervical nodes such
as the jugular or spinal accessory chains, which were then subdivided into superficial

1365

1366

Bryson et al

or deep, upper or lower, and medial or lateral subgroups. With the development of
more advanced surgical approaches to head and neck cancer, including techniques
such as selective neck dissections, a less cumbersome scheme was needed that
could accurately reflect patterns of lymphatic drainage and standardize communication between clinicians. Building on the work of earlier investigators such as
Lindberg18 and Shah and colleagues,19 the American Head and Neck Society
(AHNS) and American Academy of OtolaryngologyHead and Neck Surgery developed a 6-level system of nodal classification.2022 Some of the surgical boundaries
initially defined proved difficult to define by imaging; therefore, surrogate landmarks
were identified and an imaging-based classification of cervical lymph nodes was
developed.23 The most recent AHNS consensus statement on nodal classification
has been updated to reflect this system and the role of imaging in evaluating cervical
lymph nodes in the setting of head and neck cancer.24 The result has been a widely
accepted division of cervical lymph nodes into 7 numbered nodal levels with welldefined anatomic boundaries that can be easily identified by both surgeons and radiologists (Fig. 2).
On cross-sectional imaging, level I lymph nodes are found inferior to the myelohyoid
muscle, anterior to a line drawn at the posterior margin of the submandibular glands
and within the boundaries of the mandible. This region can be subdivided into levels
IA and IB by the anterior bellies of the digastric muscles, with level IA lymph nodes
medial and level IB nodes lateral to the anterior belly of the digastric muscle.
Level II lymph nodes are found posterior to the line drawn at the posterior margin of
the submandibular glands, anterior to the posterior margin of the sternocleidomastoid
muscle and between the lower margin of the hyoid bone and the skull base (Fig. 3).
Level II nodes can also be subdivided into levels IIA and IIB, with level IIA nodes along
the internal jugular vein and level IIB nodes posterior to the internal jugular vein and
separated by a fat plane.
Level III lymph nodes are found lateral to the carotid arteries, anterior to the posterior margin of the sternocleidomastoid muscle and between the lower margin of the
hyoid bone and lower margin of the cricoid cartilage (see Fig. 3).

Fig. 2. Cervical lymph nodes divided into 7 levels, with subdivision of levels I, II, and V.

Cervical Lymph Node Evaluation and Diagnosis

Fig. 3. Extensive cervical lymphadenopathy in a patient with non-Hodgkin lymphoma. (A)


Axial CT image with horizontal lines demarcating the posterior margins of the submandibular glands and sternocleidomastoid (SCM) muscles. These lines separate lymph nodes
within levels I (white arrow), II (black arrow), and V (white arrowhead). (B) Coronal CT image
with horizontal lines demarcating the levels of the hyoid bone and cricoid cartilage. These
lines separate lymph nodes within levels II (white arrows), III (black arrow), and IV (white
arrowheads). An intraparotid node is also seen (black arrowhead). The white rectangle
demarcates where level VII nodes would be seen. (C) Axial CT image with oblique lines
demarcating the plane between the posterior margins of the SCM and anterior scalene
muscles. These lines separate lymph nodes within levels IV (white arrows) and V (black
arrow). The white rectangle demarcates where level VI nodes would be seen.

Level IV lymph nodes are found lateral to the carotid arteries, anterior to the line connecting the posterior margins of the sternocleidomastoid and anterior scalene
muscles and between the lower margin of the cricoid cartilage and the clavicle
(see Fig. 3).

1367

1368

Bryson et al

Level V lymph nodes are found posterior to the posterior margin of the sternocleidomastoid muscle from the skull base to the clavicle. Level V nodes can be subdivided in to
levels VA and VB, with level VA nodes located between the skull base and lower margin
of the cricoid cartilage and level VB nodes located between the lower margin of the
cricoid and the clavicle anterior to the anterior margin of the trapezius muscle (see Fig. 3).
Levels VI and VII are outside the traditional boundaries of the radical neck dissection
and, although they have been defined in the literature, may be less widely applied in
clinical practice. Level VI lymph nodes encompass those found in the anterior central
or visceral compartment medial to the carotid arteries and between the lower margin
of the hyoid bone and the upper margin of the manubrium. Level VII lymph nodes
encompass those found in a paratracheal location medial to the carotid arteries within
the superior mediastinum between the upper margin of the manubrium and the innominate artery (see Fig. 3).
Some nodal sites, such as the nodal groups of the superior pericervical region including
intraparotid, buccinator, suboccipital, and retroauricular lymph nodes, lie outside these
defined levels and retain their traditional anatomic descriptors. Nodes found medial to
the carotid arteries superior to the hyoid bone are referred to as retropharyngeal nodes
(Rouvie`re), a similar example of an anatomically named nodal distribution.
PATTERNS OF NODAL DRAINAGE

The 7-level nodal classification system was designed to reflect common patterns of
lymphatic drainage, and most malignancies of the head and neck have a predictable
pattern of metastasis along these routes. Although the detailed anatomy of the
lymphatic system of the head and neck and upper aerodigestive tract is beyond the
scope of this review, recent works have mapped lymphatic drainage patterns25 and
these anatomic pathways have been found to mirror clinical experience in patterns
of metastatic disease in a variety of head and neck malignancies.2628 The presence
of predictable drainage patterns, particularly in the case of HNSCC, have led to the
clinical practice of selective neck dissection involving nodal groups at highest risk
rather than more comprehensive, and morbid, radical neck dissection. Therefore,
a basic understanding of these patterns is essential when evaluating cervical lymph
nodes in the setting of malignancy either clinically or by imaging. However, these
patterns are not immutable, and skip metastasis to more distal nodal groups without
involvement of usual proximal drainage pathways can occur in up to 15% of cases.29
Oral Cavity Lymphatic Drainage

Lymphatic drainage of the oral cavity may extend from level I to level IV, depending on
the location of the primary tumor. Anterior regions including the anterior floor of mouth,
anterior mandibular gingival, and medial lower lip drain preferentially to level IA nodes,
with the upper lip, lateral lower lip, buccal mucosal, and contiguous mucosa of the
anterior palate draining preferentially to level IB nodes. The posterior portions of the
oral cavity drain preferentially to level II.
Tongue Lymphatic Drainage

Drainage of the tongue is complex, with the ventral tongue following drainage patterns
of the floor of mouth to level IA anteromedially and IB laterally (Fig. 4). The dorsal oral
tongue may drain either to level I nodes medially or level II nodes laterally. The tongue
base shows drainage patterns more akin to pharyngeal drainage, primarily involving
levels II and III (Fig. 5). Level IV nodes may be involved in advanced disease, or via
alternative drainage pathways. Midline lesions may have bilateral drainage patterns.

Cervical Lymph Node Evaluation and Diagnosis

Fig. 4. Abnormal level Ib lymph node (white arrow) in a patient with SCC of the anterior
lateral floor of mouth involving the oral tongue. This node is borderline by size criteria,
but abnormally rounded and centrally nonenhancing.

Nasopharynx Lymphatic Drainage

The nasopharynx is richly supplied with lymphatics and shows one of the highest rates
of nodal metastasis when involved with SCC.30 The nasopharynx also serves as the
catchment basin for lymphatic drainage of most of the nasal cavity and paranasal
sinuses. The predominant lymphatic drainage pattern for these regions is to lateral

Fig. 5. Abnormal level IIa and level IIb lymph nodes (black arrows and white arrowhead, respectively) in a patient with a large tongue base SCC extending into the vallecula (white arrows).
These nodes are abnormally enlarged and heterogeneously enhancing. Borderline enlarged
right level II lymph nodes were also seen in this patient, whose tumor crossed midline.

1369

1370

Bryson et al

retropharyngeal nodes and level II nodes, with drainage to more distal level III and IV
nodal groups in more advanced disease and through alternative drainage patterns
(Fig. 6). Unlike other areas of the pharyngeal mucosa, nasopharyngeal lesions may
drain posteriorly to level V. Midline lesions of the nasopharynx may result in bilateral
drainage patterns.
Oropharyngeal Lymphatic Drainage

Oropharyngeal structures, including the soft palate, palatine and lingual tonsils, and
posterior pharyngeal wall show a similar drainage pattern to that previously described
for the tongue base. Drainage is primarily to level II and III nodal groups, with less
common involvement of retropharyngeal and level IV nodes.
Hypopharynx Lymphatic Drainage

The hypopharynx is surpassed only by the nasopharynx in density of lymphatic


drainage, with particularly dense confluence of lymphatic drainage in the piriform

Fig. 6. Extensive lymphadenopathy in a patient with nasopharyngeal carcinoma. (A) Axial


T2-weighted MRI shows bilateral retropharyngeal lymph node enlargement (black arrows).
(B) Axial unenhanced T1-weighed MRI and (C) axial T1-weighted postgadolinium MRI show
abnormal enhancement of these retropharyngeal nodes (black arrows). (D) Coronal postgadolinium fat-suppressed T1-weighted image shows bilateral retropharyngeal lymph nodes
(black arrows), extensive right level II and III lymph nodes (black arrowheads), and the
primary nasopharyngeal carcinoma (white arrows).

Cervical Lymph Node Evaluation and Diagnosis

sinuses. Drainage of the hypopharynx is similar to that of the oropharynx, with


predominant involvement of levels II to IV and occasional drainage to retropharyngeal
nodes from the posterior hypopharyngeal wall. Anterior hypopharyngeal lymphatic
drainage channels may directly communicate with laryngeal lymphatics, with eventual
involvement of level VI nodes.
Laryngeal Lymphatic Drainage

Laryngeal drainage patterns can be divided into supraglottic, glottic, and subglottic
patterns. Supraglottic structures, including the epiglottis and aryepiglottic folds, drain
primarily to level III, with occasional drainage cephalad to level II. Prominent horizontal
drainage patterns lead to an increased risk for bilateral metastasis. Glottic structures
such as the true vocal fold and vocal ligaments have poor lymphatic drainage, making
nodal metastasis from small glottic lesions less likely. More advanced glottic lesions,
with involvement of the muscles of phonation, may have involvement of nodal levels
II to IV and VI (Fig. 7). Subglottic processes have primarily lateral drainage to levels III
and IV.
Paratracheal Lymphatic Drainage

Processes involving the cervical esophagus, thyroid and parathyroid glands, and some
subglottic locations show primarily paratracheal drainage to levels VI and VII. Other less
common processes, including malignant melanoma and other cutaneous malignancies,
have less predictable patterns of metastases. Melanoma may initially involve superficial
nodes such as postauricular or suboccipital nodal groups, with additional involvement of
posterior level V nodes depending on the location of the primary lesion.31,32
IMAGING CHARACTERISTICS OF PATHOLOGIC LYMPH NODES
Size

Size criteria are widely used in evaluating lymph nodes on cross-sectional imaging
and are integral to the AJCC nodal staging system. Criteria for nodal enlargement
have been studied by multiple groups advocating different techniques and cutoff
values, with variability in the resulting sensitivity and specificity for detecting

Fig. 7. Peripherally enhancing anterior level VI (Delphian, arrow) and right level IV/V lymph
nodes (arrow head) in a patient with laryngeal carcinoma.

1371

1372

Bryson et al

malignancy.13,3335 Nodes may be measured in either greatest diameter (long axis) or


minimal diameter (short axis). Nodes measuring greater than 1.5 cm in greatest diameter in levels I or II and greater than 1.0 cm in all other levels are considered abnormal
and harbor metastatic disease in approximately 80% of cases.36 Other investigators
claim minimal diameter measurements are more accurate and reproducible on both
CT and US, with diameters exceeding 11 mm in levels I and II or 10 mm elsewhere
considered abnormal.37 Nodes meeting these minimal diameter criteria harbor metastatic disease in approximately 75% of cases.13 Retropharyngeal nodes have been
considered separately by some investigators, with those exceeding 6 to 8 mm in greatest diameter concerning for metastasis, particularly in the setting of nasopharyngeal
tumors.38,39 Some investigators have suggested alternative measurement criteria for
sonography, considering minimum diameter measurements greater than 6 to 7 mm
in levels I and II or 5 mm in levels III and IV abnormal.40
Shape

Size criteria alone may misinterpret reactive nodes as malignant and overlook small
metastases. Therefore, additional morphologic criteria have been proposed. Normal
lymph nodes tend to be flat or kidney-beanshaped, with a fat-containing hilum.
Malignant nodes typically show a rounded shape, with loss of the normal fatty hilum
or focal cortical expansion (Fig. 8).41,42 It has been suggested that a maximal diameter/minimal diameter ratio greater than 2 favors benign nodes and a ratio less than
2 favors malignancy.36,43 Nodal grouping can also help identify pathologic nodes.
Grouping refers to 3 or more nodes in continuity with each other, each measuring at
least 8 to 10 mm in diameter. Although not individually enlarged by these criteria,
groupings of nodes such as this along the expected drainage pathway for a known
malignancy are concerning and increase sensitivity for metastases.13
Density

Nodal necrosis, with its focal central hypodensity on CT and thick rind of surrounding
enhancing tissue, is an important diagnostic criterion considered virtually pathognomonic for metastatic disease in patients with HNSCC. Similar imaging findings
can be seen on MRI, including a focal defect in enhancement centrally on
gadolinium-enhanced T1-weighted imaging. This nonenhancing central region is typically hyperintense on fat-suppressed T2-weighted images, but may show variable

Fig. 8. Abnormal level III lymph nodes in a patient with metastatic papillary thyroid carcinoma. (A) Gray-scale sonographic image showing the rounded shape of 2 lymph nodes
with abnormal maximal diameter/minimal diameter ratio. (B) Color Doppler sonographic
image showing loss of the normal fatty hilum and normal hilar vasculature. Peripheral blood
flow is seen.

Cervical Lymph Node Evaluation and Diagnosis

signal characteristics depending on the makeup of the necrotic tissue (Fig. 9).
Although it is difficult to apply these characteristics to small foci of necrosis less
than 3 mm in size, they are generally accurate in detecting necrotic nodes, with sensitivities of 91% and 93% and specificities of 93% and 89% for CT and MRI, respectively.44 Although some studies have suggested that CT is superior to MRI in
detection of central nodal necrosis, both have been shown to be more sensitive
than US.44,45 Central nodal necrosis is more common in larger nodes, occurring in
56% to 63% of metastatic nodes larger than 1.5 cm and 10% to 33% of nodes smaller
than 1 cm; however, as many as 35% of all necrotic nodes are less than 1 cm in
size.33,34,46 Rarely, metastatic lymph nodes may appear cystic, with central fluid characteristics and a thin rim of tissue. This situation occurs more commonly in papillary
thyroid carcinoma, but can occur in HNSCC. These cystic nodes can be misinterpreted as branchial cleft cysts, and care should be taken to evaluate for possible
primary malignancy when cystic lesions are seen in adults.47
Extracapsular Spread

Extracapsular spread of malignancy and invasion of adjacent structures are of key


clinical importance in determining a patients prognosis and surgical options. Extracapsular spread is a histologic diagnosis in many cases, with imaging features such as
blurring of nodal margins and soft tissue infiltration of adjacent fat or muscle producing
sensitivities and specificities of only 63% to 81% and 60% to 72% for CT and up to
77% and 72% for MRI, respectively (Fig. 10).4850 Other studies reported an accuracy
of 90% for CT and 78% for MRI in detecting extracapsular spread.45 When present,
findings of macroscopic extracapsular spread identifiable by imaging increase the
rate of local recurrence by a factor of 3.5 compared with those without evidence of
extracapsular nodal disease.51 In addition, if 2 or more nodes show extracapsular
spread, the risk of local recurrence is 58.3%, rate of distant metastases is 33.3%,
and median survival is less than 1 year.52 Larger nodes are more likely to show extracapsular spread of disease, with up to 75% of nodes greater than 3 cm in size showing
evidence either by imaging or microscopically.

Fig. 9. Abnormal right level II lymph node in a patient with SCC of the right tonsil. (A) Axial
T2-weighted MRI image shows increased signal within this necrotic lymph node (white
arrow). (B) Axial postgadolinium fat-suppressed T1-weighted image shows thick irregular
peripheral enhancement of this node consistent with nodal necrosis (white arrow).

1373

1374

Bryson et al

Fig. 10. Enlarged right level II lymph node in a patient with SCC of unknown primary site
(arrow). Poor definition of the lateral node margin and stranding of adjacent fat are consistent with extracapsular spread of neoplasm.

Invasion of Adjacent Structures

When nodal disease is advanced, confluent masses of cervical adenopathy may


invade adjacent structures such as the carotid artery or jugular vein. Carotid invasion
in most cases renders the mass unresectable, and further preoperative testing, such
as balloon occlusion testing, may be required if carotid sacrifice is to be considered.
Fat planes separating an infiltrating mass from the vessels should be evaluated to
determine the degree of circumferential involvement. If less than 180 of the vessel
circumference is involved, then direct vascular invasion is unlikely. However, if
greater than 270 of circumferential encasement is present by cross-sectional
imaging, arterial wall invasion can be presumed with a relatively high degree of sensitivity and specificity (Fig. 11).53 Maneuvers on real-time sonography to determine
mobility of a mass relative to vessels can also be useful to determine if vessel invasion has occurred.54
ADVANCED IMAGING TECHNIQUES
Contrast-Enhanced CT

Traditionally, cross-sectional anatomic imaging with CT, MRI, or US has formed the
cornerstone of head and neck imaging, with the choice of initial imaging modality
depending on the individual center and clinical indication. Contrast-enhanced CT is
widely used because of its short examination times, ubiquitous availability, high
inherent contrast between lymph nodes and cervical fat, and relatively high spatial
resolution with modern multidetector scanners. The short examination times and relatively wider gantry bore are better tolerated by claustrophobic patients compared with
MRI and CT images are typically less affected by motion artifacts. MRI, with its highcontrast resolution and multiplanar imaging capabilities, can also readily detect
abnormal lymph nodes, and modern turbospin echo sequences have shortened

Cervical Lymph Node Evaluation and Diagnosis

Fig. 11. Confluent lymphadenopathy causing vascular encasement in a patient with unresectable oropharyngeal SCC. (A) Confluent level II adenopathy with encasement of the
left internal carotid (white arrow) and external carotid (black arrow) arteries. (B) Additional
confluent level III adenopathy with resultant encasement of the left common carotid artery
(white arrowhead).

examination times. MRI has added value in evaluating a primary neoplastic process,
with improved detection of bone marrow involvement and perineural spread of
disease.55 Overall, most studies comparing the accuracy of CT and MRI in evaluating
the important clinically negative (N0) neck have found no significant difference
between the 2 modalities, with imaging detecting approximately 40% to 60% of occult
metastases and micrometastases going largely undetected.5659
US

US, particularly in combination with ultrasound-guided fine-needle aspiration, has


gained popularity in Europe. In general, US is superior to palpation in detection of
nodal metastases and may outperform CT and MRI.5961 Doppler techniques evaluating patterns of hilar and peripheral blood flow have been found to offer added value
in identifying nodal metastases.6264 Ultrasound-guided fine-needle aspiration
cytology has been shown to be superior to CT and MRI, with specificity for nodal
metastases approaching 100%.65 These techniques are highly operator dependent
and labor intensive to achieve this degree of accuracy.
Diffusion-Weighted MRI

Recently, techniques such as diffusion-weighted MRI (DWI) and perfusion have added
new tools to the imaging armamentarium. HNSCC can show areas of restricted diffusion and corresponding decreased signal on apparent diffusion coefficient maps,
likely because of their highly cellular nature.66 Several studies have now shown that
DWI can aid in differentiation of benign reactive lymphadenopathy from metastatic
malignancy and may be particularly helpful in evaluating the posttreatment neck
(Fig. 12).6769 These studies have shown sensitivities of 84% to 89%, specificities of
94% to 97%, and accuracy of 91% to 94% for detection of metastatic lymph nodes
by DWI, significantly outperforming conventional turbospin echo imaging in each

1375

1376

Bryson et al

Fig. 12. Metastatic lymph nodes in a patient with tongue base SCC on T2 and DWI. (A) Axial
fat-suppressed T2-weighted MRI shows irregular left tongue base mass (black arrow) and
bilateral abnormal level II lymph nodes (white arrows). A small focus of increased T2 signal
is seen within one of the nodes (white arrowhead) (B) Axial DWI at a corresponding level
shows impeded diffusion within the primary tumor (black arrow) and within bilateral metastatic lymph nodes (white arrows). Note the small focus of necrosis within the right-sided
node does not impede diffusion (white arrowhead).

case. As with other modalities, DWI sensitivity for metastatic disease decreases to
76% in subcentimeter nodal metastases. This technique is still not standardized,
and these values are dependent on the apparent diffusion coefficient cutoff values
chosen. Also, magnetic field inhomogeneity or improper coil placement can negatively
affect image quality and limit diagnostic usefulness.70
Contrast-Enhanced CT and MRI

The role of contrast-enhanced imaging in CT and MRI is well established. Iodinated


contrast enables evaluation of nodal architecture by CT and is required for identification of nodal necrosis in most cases. Gadolinium contrast media may be less integral
to the evaluation of cervical lymph nodes by MRI, but add value in evaluating for nodal
necrosis and in evaluating characteristics of the primary lesion, such as perineural
spread of malignancy.71 Newer contrast-enhanced techniques, such as perfusion
imaging, are now being used to provide functional evaluations of cervical lymph
nodes. Perfusion techniques evaluate dynamic microscopic blood flow changes by
documenting changes in signal intensity (MRI) or attenuation (CT) in a given region
of interest after bolus administration of contrast material. These techniques, like
DWI, are noninvasive and can be obtained without adding significant additional time
to imaging protocols.72 CT perfusion characteristics of neoplastic tissue have been
shown to be different from adjacent normal tissue, with SCC of the upper aerodigestive tract showing increased blood volume and blood flow, with corresponding
decreases in mean transit time (Fig. 13).73 Perfusion characteristics may be able to
direct therapy, with some studies linking increased blood volume/flow with increased
chemosensitivity.74 Although some studies have suggested that CT perfusion was not
useful when applied to lymph nodes,75 more recent studies have shown that these
perfusion techniques can be applied to help differentiate metastatic nodes from reactive benign lymph nodes.76 Similarly, recent studies of dynamic susceptibilityweighted perfusion MRI have shown promise in differentiating metastases from
benign lymph nodes and may be able to differentiate between metastases and
lymphoma.77

Cervical Lymph Node Evaluation and Diagnosis

Fig. 13. CT perfusion imaging of a metastatic right level II lymph node. (A) Axial contrastenhanced CT image obtained during perfusion imaging shows peripheral enhancement
of this abnormal lymph node (white arrows). Corresponding increases (red on the color
scale) in blood volume (B) and blood flow (C) are seen on perfusion maps at the periphery
of this node.

POSITRON EMISSION TOMOGRAPHY AND [18F]FLUORODEOXYGLUCOSE POSITRON


EMISSION TOMOGRAPHY

Positron emission tomography (PET) with [18F]fluorodeoxyglucose (FDG), and modern


fused PET/CT, are powerful tools that are able to evaluate glucose metabolism within
cervical lymph nodes. This ability to provide metabolic information, and now fuse it
with anatomic imaging, has proved powerful, with FDG-PET and PET/CT routinely outperforming conventional CT and MRI in the detection of nodal disease in patients who
have head and neck cancer.7881 PET imaging in these studies has shown sensitivity for
nodal metastases of up to 90% and specificity approaching 100%. Although the technical resolution of PET imaging is 4 to 5 mm and micrometastases remain a significant
challenge, FDG-PET is capable of detecting metastases within lymph nodes of 4 to
6 mm, which would be overlooked by anatomic imaging alone.78,82,83 Current practice
does not use PET/CT routinely for initial staging; however, it has the capability to alter
therapy through detection of previously occult nodal and distant metastases and can
provide functional information about the primary lesion (Fig. 14). Primary tumors, but
not metastatic lymph nodes, with higher objective measures of metabolic activity
(higher standardized uptake values) have been shown to have higher rates of locoregional recurrence and may benefit from more aggressive therapy.84 Some investigators

1377

1378

Bryson et al

Fig. 14. Staging study with FDG-PET/CT. (A) Hypermetabolic right pyriform sinus SCC with
regional right level III nodal metastasis. (B) Whole-body PET/CT imaging can detect distant
metastases, as in this case of hypermetabolic mediastinal lymph nodes concerning for
distant metastases.

have suggested that a negative PET examination can decrease the risk of occult metastases in clinically N0 patients with T1 to T3 primary tumors to 15% or less, a rate at which
elective nodal treatments may be deferred.80 In the posttherapy neck, PET has proved
superior to CT or MRI in detecting residual nodal metastases.85
SUMMARY AND RECOMMENDATIONS

Cross-sectional imaging, particularly CT and MRI, is a valuable tool in the armamentarium of the head and neck surgeon for evaluation of cervical lymph nodes, particularly in the setting of head and neck malignancies. The evaluation of nodal size,
morphology, and enhancement characteristics is the primary means of identifying
abnormal lymph nodes on cross-sectional imaging, and understanding the nodal classification scheme is required to effectively communicate the location of abnormal
nodes to other physicians. Imaging techniques outperform the clinical examination
in detection of metastatic lymph nodes and can detect 40% to 60% of occult metastatic disease, but continue to be insensitive for detection of micrometastases. Newer
techniques such as DWI, perfusion imaging, and FDG-PET/CT may improve the
imaging evaluation of the N0 neck.
REFERENCES

1. Lazor JB, et al. Comparison of computed tomography and surgical findings in


deep neck infections. Otolaryngol Head Neck Surg 1994;111(6):74650.
2. Smith JL 2nd, Hsu JM, Chang J. Predicting deep neck space abscess using
computed tomography. Am J Otolaryngol 2006;27(4):2447.
3. McKellop JA, Bou-Assaly W, Mukherji SK. Emergency head & neck imaging:
infections and inflammatory processes. Neuroimaging Clin North Am 2010;
20(4):65161.
4. Sidell DR, Shapiro NL. Diagnostic accuracy of ultrasonography for midline neck
masses in children. Otolaryngol Head Neck Surg 2011;144(3):4314.
5. Byers RM, Wolf PF, Ballantyne AJ. Rationale for elective modified neck dissection.
Head Neck Surg 1988;10(3):1607.
6. Giacomarra V, et al. Predictive factors of nodal metastases in oral cavity and
oropharynx carcinomas. Laryngoscope 1999;109(5):7959.

Cervical Lymph Node Evaluation and Diagnosis

7. Edge SB. American Joint Committee on Cancer and American Cancer Society.
AJCC cancer staging handbook from the AJCC cancer staging manual. New
York: Springer; 2010. p. 1 online resource (xix, 718 p).
8. Layland MK, Sessions DG, Lenox J. The influence of lymph node metastasis in
the treatment of squamous cell carcinoma of the oral cavity, oropharynx, larynx,
and hypopharynx: N0 versus N1. Laryngoscope 2005;115(4):62939.
9. Haberal I, et al. Which is important in the evaluation of metastatic lymph nodes in
head and neck cancer: palpation, ultrasonography, or computed tomography?
Otolaryngol Head Neck Surg 2004;130(2):197201.
10. Alderson DJ, et al. Observer error in the assessment of nodal disease in head
and neck cancer. Head Neck 2001;23(9):73943.
11. Atula TS, et al. Assessment of cervical lymph node status in head and neck
cancer patients: palpation, computed tomography and low field magnetic resonance imaging compared with ultrasound-guided fine-needle aspiration cytology.
Eur J Radiol 1997;25(2):15261.
12. Weiss MH, Harrison LB, Isaacs RS. Use of decision analysis in planning
a management strategy for the stage N0 neck. Arch Otolaryngol Head Neck
Surg 1994;120(7):699702.
13. van den Brekel MW, et al. Cervical lymph node metastasis: assessment of radiologic criteria. Radiology 1990;177(2):37984.
14. Brennan JA, et al. Molecular assessment of histopathological staging in
squamous-cell carcinoma of the head and neck. N Engl J Med 1995;332(7):
42935.
15. Hamakawa H, et al. Keratin mRNA for detecting micrometastasis in cervical
lymph nodes of oral cancer. Cancer Lett 2000;160(1):11523.
16. Braunius WW, et al. Observing stage-shifts in head and neck squamous cell
carcinoma from initial clinical outpatient staging to definite clinical tumour board
staging using radiological and endoscopical investigations: will less do? Clin
Otolaryngol 2011;36(4):35260.
17. Rouvie`re H, Tobias MJ. Anatomy of the human lymphatic system. Ann Arbor (MI):
Edwards brothers, inc; 1938. ix, p. 318.
18. Lindberg R. Distribution of cervical lymph node metastases from squamous cell
carcinoma of the upper respiratory and digestive tracts. Cancer 1972;29(6):
14469.
19. Shah JP, et al. Surgical grand rounds. Neck dissection: current status and future
possibilities. Clin Bull 1981;11(1):2533.
20. Robbins KT, et al. Standardizing neck dissection terminology. Official report of the
Academys Committee for Head and Neck Surgery and Oncology. Arch Otolaryngol Head Neck Surg 1991;117(6):6015.
21. Robbins KT. Classification of neck dissection: current concepts and future
considerations. Otolaryngol Clin North Am 1998;31(4):63955.
22. Robbins KT, et al. Neck dissection classification update: revisions proposed by
the American Head and Neck Society and the American Academy of
Otolaryngology-Head and Neck Surgery. Arch Otolaryngol Head Neck Surg
2002;128(7):7518.
23. 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):38896.
24. Robbins KT, et al. Consensus statement on the classification and terminology of neck dissection. Arch Otolaryngol Head Neck Surg 2008;134(5):
5368.

1379

1380

Bryson et al

25. Werner JA, Dunne AA, Myers JN. Functional anatomy of the lymphatic drainage
system of the upper aerodigestive tract and its role in metastasis of squamous
cell carcinoma. Head Neck 2003;25(4):32232.
26. de Wilt JH, et al. Correlation between preoperative lymphoscintigraphy and metastatic nodal disease sites in 362 patients with cutaneous melanomas of the head
and neck. Ann Surg 2004;239(4):54452.
27. King AD, et al. Neck node metastases from nasopharyngeal carcinoma: MR
imaging of patterns of disease. Head Neck 2000;22(3):27581.
28. Shah JP. Patterns of cervical lymph node metastasis from squamous carcinomas
of the upper aerodigestive tract. Am J Surg 1990;160(4):4059.
29. Byers RM, et al. Frequency and therapeutic implications of skip metastases in the
neck from squamous carcinoma of the oral tongue. Head Neck 1997;19(1):149.
30. Wang Y, Ow TJ, Myers JN. Pathways for cervical metastasis in malignant
neoplasms of the head and neck region. Clin Anat 2012;25(1):5471.
31. Pathak I, et al. Do nodal metastases from cutaneous melanoma of the head and
neck follow a clinically predictable pattern? Head Neck 2001;23(9):78590.
32. Wagner JD, et al. Cervical sentinel lymph node biopsy for melanomas of the head
and neck and upper thorax. Arch Otolaryngol Head Neck Surg 2000;126(3):
31321.
33. Don DM, et al. Evaluation of cervical lymph node metastases in squamous cell
carcinoma of the head and neck. Laryngoscope 1995;105(7 Pt 1):66974.
34. Friedman M, et al. Nodal size of metastatic squamous cell carcinoma of the neck.
Laryngoscope 1993;103(8):8546.
35. van den Brekel MW, Castelijns JA, Snow GB. The size of lymph nodes in the neck
on sonograms as a radiologic criterion for metastasis: how reliable is it? AJNR Am
J Neuroradiol 1998;19(4):695700.
36. Som PM. Detection of metastasis in cervical lymph nodes: CT and MR criteria and
differential diagnosis. AJR Am J Roentgenol 1992;158(5):9619.
37. Sumi M, Ohki M, Nakamura T. Comparison of sonography and CT for differentiating benign from malignant cervical lymph nodes in patients with squamous
cell carcinoma of the head and neck. AJR Am J Roentgenol 2001;176(4):
101924.
38. Mancuso AA, et al. Computed tomography of cervical and retropharyngeal lymph
nodes: normal anatomy, variants of normal, and applications in staging head and
neck cancer. Part II: pathology. Radiology 1983;148(3):71523.
39. Mancuso AA, et al. Computed tomography of cervical and retropharyngeal lymph
nodes: normal anatomy, variants of normal, and applications in staging head and
neck cancer. Part I: normal anatomy. Radiology 1983;148(3):70914.
40. Yonetsu K, et al. Contribution of doppler sonography blood flow information to the
diagnosis of metastatic cervical nodes in patients with head and neck cancer:
assessment in relation to anatomic levels of the neck. AJNR Am J Neuroradiol
2001;22(1):1639.
41. Rubaltelli L, et al. Sonography of abnormal lymph nodes in vitro: correlation of
sonographic and histologic findings. AJR Am J Roentgenol 1990;155(6):12414.
42. Vassallo P, et al. Differentiation of benign from malignant superficial lymphadenopathy: the role of high-resolution US. Radiology 1992;183(1):21520.
43. Bruneton JN, et al. Very high frequency (13 MHz) ultrasonographic examination
of the normal neck: detection of normal lymph nodes and thyroid nodules.
J Ultrasound Med 1994;13(2):8790.
44. King AD, et al. Necrosis in metastatic neck nodes: diagnostic accuracy of CT, MR
imaging, and US. Radiology 2004;230(3):7206.

Cervical Lymph Node Evaluation and Diagnosis

45. Yousem DM, et al. Central nodal necrosis and extracapsular neoplastic spread in
cervical lymph nodes: MR imaging versus CT. Radiology 1992;182(3):7539.
46. Eida S, et al. Combination of helical CT and Doppler sonography in the follow-up
of patients with clinical N0 stage neck disease and oral cancer. AJNR Am J Neuroradiol 2003;24(3):3128.
47. 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):10110, viii.
48. Carvalho P, et al. Accuracy of CT in detecting squamous carcinoma metastases
in cervical lymph nodes. Clin Radiol 1991;44(2):7981.
49. Steinkamp HJ, et al. Extracapsular spread of cervical lymph node metastases: Diagnostic value of magnetic resonance imaging. Rofo 2002;174(1):
505 [in German].
50. Steinkamp HJ, et al. The extracapsular spread of cervical lymph node
metastases: the diagnostic value of computed tomography. Rofo 1999;170(5):
45762 [in German].
51. Brasilino de Carvalho M. Quantitative analysis of the extent of extracapsular invasion and its prognostic significance: a prospective study of 170 cases of carcinoma of the larynx and hypopharynx. Head Neck 1998;20(1):1621.
52. Greenberg JS, et al. Extent of extracapsular spread: a critical prognosticator in
oral tongue cancer. Cancer 2003;97(6):146470.
53. Yousem DM, et al. Carotid artery invasion by head and neck masses: prediction
with MR imaging. Radiology 1995;195(3):71520.
54. Gritzmann N, et al. Invasion of the carotid artery and jugular vein by lymph node
metastases: detection with sonography. AJR Am J Roentgenol 1990;154(2):
4114.
55. Weber AL, Romo L, Hashmi S. Malignant tumors of the oral cavity and
oropharynx: clinical, pathologic, and radiologic evaluation. Neuroimaging Clin
North Am 2003;13(3):44364.
56. Curtin HD, et al. Comparison of CT and MR imaging in staging of neck metastases. Radiology 1998;207(1):12330.
57. Hillsamer PJ, et al. Improving diagnostic accuracy of cervical metastases with
computed tomography and magnetic resonance imaging. Arch Otolaryngol
Head Neck Surg 1990;116(11):1297301.
58. Lenz M, Kersting-Sommerhoff B, Gross M. Diagnosis and treatment of the N0
neck in carcinomas of the upper aerodigestive tract: current status of diagnostic
procedures. Eur Arch Otorhinolaryngol 1993;250(8):4328.
59. van den Brekel MW, et al. Modern imaging techniques and ultrasound-guided
aspiration cytology for the assessment of neck node metastases: a prospective
comparative study. Eur Arch Otorhinolaryngol 1993;250(1):117.
60. Prayer L, et al. Sonography versus palpation in the detection of regional lymphnode metastases in patients with malignant melanoma. Eur J Cancer 1990;26(7):
82730.
61. Vassallo P, et al. In-vitro high-resolution ultrasonography of benign and malignant
lymph nodes. A sonographic-pathologic correlation. Invest Radiol 1993;28(8):
698705.
62. Ahuja AT, Ying M. Sonographic evaluation of cervical lymph nodes. AJR Am J
Roentgenol 2005;184(5):16919.
63. Ariji Y, et al. Power Doppler sonography of cervical lymph nodes in patients with
head and neck cancer. AJNR Am J Neuroradiol 1998;19(2):3037.
64. Tschammler A, et al. Vascular patterns in reactive and malignant lymphadenopathy. Eur Radiol 1996;6(4):47380.

1381

1382

Bryson et al

65. van den Brekel MW, et al. Occult metastatic neck disease: detection with US
and US-guided fine-needle aspiration cytology. Radiology 1991;180(2):
45761.
66. Wang J, et al. Head and neck lesions: characterization with diffusion-weighted
echo-planar MR imaging. Radiology 2001;220(3):62130.
67. Dirix P, et al. Diffusion-weighted MRI for nodal staging of head and neck squamous cell carcinoma: impact on radiotherapy planning. Int J Radiat Oncol Biol
Phys 2010;76(3):7616.
68. Holzapfel K, et al. Value of diffusion-weighted MR imaging in the differentiation
between benign and malignant cervical lymph nodes. Eur J Radiol 2009;72(3):
3817.
69. Vandecaveye V, et al. Head and neck squamous cell carcinoma: value of
diffusion-weighted MR imaging for nodal staging. Radiology 2009;251(1):
13446.
70. Hermans R, Vandecaveye V. Diffusion-weighted MRI in head and neck cancer.
Cancer Imaging 2007;7:1267.
71. Hudgins PA. Contrast enhancement in head and neck imaging. Neuroimaging
Clin North Am 1994;4(1):10115.
72. Shah GV, et al. New directions in head and neck imaging. J Surg Oncol 2008;
97(8):6448.
73. Gandhi D, et al. Computed tomography perfusion of squamous cell carcinoma of
the upper aerodigestive tract. Initial results. J Comput Assist Tomogr 2003;27(5):
68793.
74. Zima A, et al. Can pretreatment CT perfusion predict response of advanced
squamous cell carcinoma of the upper aerodigestive tract treated with induction
chemotherapy? AJNR Am J Neuroradiol 2007;28(2):32834.
75. Bisdas S, et al. Quantitative measurements of perfusion and permeability of
oropharyngeal and oral cavity cancer, recurrent disease, and associated lymph
nodes using first-pass contrast-enhanced computed tomography studies. Invest
Radiol 2007;42(3):1729.
76. Trojanowska A, et al. Squamous cell cancer of hypopharynx and larynxevaluation of metastatic nodal disease based on computed tomography perfusion
studies. Eur J Radiol 2011.
77. Abdel Razek AA, Gaballa G. Role of perfusion magnetic resonance imaging in
cervical lymphadenopathy. J Comput Assist Tomogr 2011;35(1):215.
78. Adams S, et al. Prospective comparison of 18F-FDG PET with conventional
imaging modalities (CT, MRI, US) in lymph node staging of head and neck
cancer. Eur J Nucl Med 1998;25(9):125560.
79. Hannah A, et al. Evaluation of 18 F-fluorodeoxyglucose positron emission tomography and computed tomography with histopathologic correlation in the initial
staging of head and neck cancer. Ann Surg 2002;236(2):20817.
80. Ng SH, et al. Prospective study of [18F]fluorodeoxyglucose positron emission
tomography and computed tomography and magnetic resonance imaging in
oral cavity squamous cell carcinoma with palpably negative neck. J Clin Oncol
2006;24(27):43716.
81. Roh JL, et al. Utility of 2-[18F] fluoro-2-deoxy-D-glucose positron emission tomography and positron emission tomography/computed tomography imaging in the
preoperative staging of head and neck squamous cell carcinoma. Oral Oncol
2007;43(9):88793.
82. Benchaou M, et al. The role of FDG-PET in the preoperative assessment of
N-staging in head and neck cancer. Acta Otolaryngol 1996;116(2):3325.

Cervical Lymph Node Evaluation and Diagnosis

83. Jabour BA, et al. Extracranial head and neck: PET imaging with 2-[F-18]fluoro-2-deoxy-D-glucose and MR imaging correlation. Radiology 1993;186(1):
2735.
84. Schwartz DL, et al. FDG-PET prediction of head and neck squamous cell cancer
outcomes. Arch Otolaryngol Head Neck Surg 2004;130(12):13617.
85. Kim SY, et al. Evaluation of 18F-FDG PET/CT and CT/MRI with histopathologic
correlation in patients undergoing salvage surgery for head and neck squamous
cell carcinoma. Ann Surg Oncol 2011;18(9):257984.

1383

También podría gustarte