Anatomy of the Lymphatic System of the Neck

The head and neck region has a rich network of lymphatic vessels draining from the base of the skull through the jugular nodes, spinal accessory nodes, and transverse cervical nodes to the venous jugulosubclavian confluence or the thoracic duct on the left side and the lymphatic duct on the right side.1,2 A comprehensive anatomic description of this network was made by Rouvière more than 50 years ago.¹ The whole lymphatic system of the neck is contained in the celluloadipose tissue delineated by the aponeurosis enveloping the muscles, vessels, and nerves (Fig. 38-1). The lymphatic drainage is mainly ipsilateral, but structures such as the soft palate, tonsils, base of the tongue, posterior pharyngeal wall, and especially the nasopharynx have bilateral drainage. On the other hand, sites such as the true vocal cord, paranasal sinuses, and middle ear have few or no lymphatic vessels at all.

Figure 38-1 Lymphatic nodes of the head and neck. Lateral view of the superficial and deep node groups of the cervicocephalic region. B, buccal node; DAJ, deep anterior jugular node; DiP, deep intraparotid node; F, facial node; iH, infrahyoid node; JD, jugulodigastric node (Kütner’s node); JO, jugulo-omohyoid node (Poirier’s node); LDC, superior (s), middle (m), and inferior (i) lateral deep cervical nodes; LsC, lateral supraclavicular node; M (pink), malar node; M (green), mastoid node; MsC, medial supraclavicular node; pA, preauricular node; PDC, superior (s), middle (m), and inferior (i) posterior deep cervical nodes; pL, prelaryngeal node; pT, pretracheal node; R, recurrent node; rPh, retropharyngeal node; sA, subauricular node; SAJ, superficial anterior jugular node; SEJ, superficial external jugular node; SiP, superficial intraparotid node; sMd, submandibular node; sMt, submental node; sO, suboccipital node; sP, subparotid node.

Adapted from Grégoire V, Scalliet P, Ang KK: Clinical Target Volumes in Conformal and Intensity Modulated Radiation Therapy: A Clinical Guide to Cancer Treatment. New York, Springer-Verlag, 2003.

The nomenclature of head and neck lymph nodes has been complicated by various confusing synonyms that are still in use in major textbooks and articles. Several expert bodies have proposed the adoption of systematic classifications aimed at standardizing the terminology. Following the description by Rouvière, the TNM (primary tumor, regional nodes, metastases) atlas proposed a terminology that divides the head and neck lymph nodes into 12 groups.³ In parallel to this classification, the Committee for Head and Neck Surgery and Oncology of the American Academy for Otolaryngology–Head and Neck Surgery has been working on a classification (the so-called Robbins classification), dividing the neck into six levels, including eight node groups.⁴ This classification is based on the description of a level system that has been used for a long time by the Head and Neck Service at the Memorial Sloan-Kettering Cancer Center (MSKCC).⁵ Because one of the objectives in developing the Robbins classification was to create a standardized system of terminology for neck dissection procedures, only the lymph node groups routinely removed during neck dissection were considered. The terminology proposed by Robbins was recommended by the International Union Against Cancer (UICC).⁶ A comparison of the TNM system and the Robbins terminology is shown in Table 38-1. The major advantage of the Robbins classification over the TNM terminology is the definition of the boundaries of the node levels. The delineation of these boundaries is based on anatomic structures such as major blood vessels, muscles, nerves, bones, and cartilage that are easily identifiable by a surgeon during neck dissection procedures. The anatomic boundaries are oriented to a patient lying in a supine position with the neck in a surgical position (i.e., hyperextension) to better individualize the anatomic structures.

TABLE 38-1 Comparison of the TNM Atlas Terminology and the Robbins Classification of the Lymph Nodes of the Neck

Level Ia is a unique median region that contains the submental nodes. The lymph nodes are located in a triangular region limited anteriorly by the platysma muscle, posteriorly by the mylohyoid muscles, cranially by the symphysis of the mandible, caudally by the hyoid bone, and laterally by the anterior belly of the digastric muscle. The medial limit of level Ia is virtual because the region continues into the contralateral level Ia. Nodes in level Ia drain the skin of the chin, mid lower lip, tip of the tongue, and anterior floor of the mouth. Level Ia is at greatest risk for harboring metastases from cancer arising from the floor of the mouth, anterior oral tongue, anterior mandibular alveolar ridge, and lower lip.

Level Ib contains the submandibular nodes. It is located within the boundaries of the anterior and posterior belly of the digastric muscle, the stylohyoid muscle, and the body of the mandible. It is limited anteriorly by the stylohyoid muscle, posteriorly by a vertical plane defined by the spinal accessory nerve, medially (deeply) by the anterior belly of the digastric muscle, and laterally (superficially) by the basilar border of the mandible. Cranially, it is limited by the basilar border of the mandible and caudally, by the posterior belly of the digastric muscle. The submandibular nodes receive efferent lymphatics from the submental lymph nodes, medial canthus, lower nasal cavity, hard and soft palate, maxillary and mandibular alveolar ridges, cheek, upper and lower lips, and most of the anterior tongue. Nodes in level Ib are at risk for developing metastases from cancers of the oral cavity, anterior nasal cavity, soft tissue structures of the midface, and submandibular gland.

Level II contains the upper jugular lymph nodes located around the upper one-third of the internal jugular vein and upper spinal accessory nerve. It extends from the level of the skull base to the carotid bifurcation (a surgical landmark) or the caudal border of the body of the hyoid bone (a clinical landmark). Level II is limited cranially by the insertion of the posterior belly of the digastric muscle to the mastoid, caudally by the caudal border of the body of the hyoid bone, anteriorly by the stylohyoid muscle, posteriorly by the posterior edge of the sternocleidomastoid muscle, medially by the carotid artery and paravertebral muscles (levator scapulae and splenius capitis), and laterally by the sternocleidomastoid and platysma muscles. Level II is further subdivided into two compartments. The lymph nodes located anterior to a vertical plane defined by the upper third of the spinal accessory nerve are included in level IIa, whereas the lymph nodes located posterior to the spinal accessory nerve are included in level IIb. Level II receives efferent lymphatics from the face, parotid gland, and submandibular, submental, and retropharyngeal nodes. Level II also directly receives the collecting lymphatics from the nasal cavity, pharynx, larynx, external auditory canal, middle ear, and sublingual and submandibular glands. The nodes in level II are therefore at greatest risk for harboring metastases from cancers arising from the nasal cavity, oral cavity, nasopharynx, oropharynx, hypopharynx, larynx, and major salivary glands. Level IIb is more likely associated with primary tumors arising in the oropharynx or nasopharynx and is less frequently involved in tumors of the oral cavity, larynx, or hypopharynx.

Level III contains the middle jugular lymph nodes located around the middle third of the internal jugular vein. It is the caudal extension of level II. It is limited cranially by the caudal border of the body of the hyoid bone and caudally by a plane in which the omohyoid muscle crosses the internal jugular vein (a surgical landmark) or by the caudal border of the cricoid cartilage (a clinical landmark). The anterior limit is the lateral edge of the sternohyoid muscle, and the posterior limit is the posterior border of the sternocleidomastoid muscle. Laterally, level III is limited by the sternocleidomastoid muscle and medially by the internal carotid artery and paraspinal muscles. Level III contains a highly variable number of lymph nodes and receives efferent lymphatics from levels II and V and some efferent lymphatics from the retropharyngeal, pretracheal, and recurrent laryngeal nodes. It collects the lymphatics from the base of the tongue, tonsils, larynx, hypopharynx, and thyroid gland. Nodes in level III are at greatest risk for harboring metastases from cancers of the oral cavity, nasopharynx, oropharynx, hypopharynx, and larynx.

Level IV includes the lower jugular lymph nodes located around the inferior third of the internal jugular vein from the caudal limit of level III to the clavicle caudally. The anterior and posterior limits are the same as for level III (i.e., the lateral border of the sternohyoid muscle and the posterior edge of the sternocleidomastoid muscle, respectively). Laterally, level IV is limited by the sternocleidomastoid muscle and medially by the internal carotid artery and paraspinal muscles. Level IV contains a variable number of nodes and receives efferent lymphatics primarily from levels III and V; some efferent lymphatics from the retropharyngeal, pretracheal, and recurrent laryngeal nodes; and collecting lymphatics from the hypopharynx, larynx, and thyroid gland.¹ Level IV nodes are at high risk for harboring metastases from cancers of the hypopharynx, larynx, and cervical esophagus.

Level V includes the lymph nodes of the posterior triangle group. This group includes the lymph nodes located along the lower part of the spinal accessory nerve and the transverse cervical vessels. Level V is limited cranially by the convergence of the sternocleidomastoid muscle and the trapezius muscles, caudally by the clavicle, anteriorly by the posterior border of the sternocleidomastoid muscle, and posteriorly by the anterior border of the trapezius muscle. Laterally, level V is limited by the platysma muscle and the skin and medially by the splenius capitis, levator scapulae, and scaleni (posterior, medial, and anterior) muscles. Level V is currently subdivided into levels Va and Vb. The distinction between the upper posterior triangle (level Va) and the lower posterior triangle (level Vb) allows lymph node involvement of the lower two-thirds of the spinal accessory nerve chain to be differentiated from that of the transverse cervical vessel chain.7,8 A horizontal plane defined by the caudal edge of the cricoid cartilage separates these two compartments. The demarcation between the posterior end of level IIb and the uppermost part of level Va has still not been clearly defined. The American Academy for Otolaryngology–Head and Neck Surgery defined the posterior boundary of level IIb as the posterior border of the sternocleidomastoid muscle and the apex of the convergence of the sternocleidomastoid muscle and the trapezius muscles as the cranial boundary of level Va. However, the uppermost part of level Va contains superficial occipital lymph nodes and, inconsistently, one subfascial lymph node close to the occipital attachment of the sternocleidomastoid muscle.¹

These lymph nodes collect lymphatics from the occipital scalp and the postauricular and nuchal regions. They are not involved in the drainage of head and neck cancers except for skin tumors. Consequently, Hamoir and colleagues⁹ proposed to subdivide the level Va nodes into two sublevels: the apex of level V, or level Vas (superior), and level Vai (inferior). The border between level Vas and level Vai should be the lower two-thirds of the spinal accessory nerve. From a radiologic point of view, a horizontal plane defined by the upper edge of the body of the hyoid bone appears to be a reliable landmark to separate the two sections. Dissection of the apex (level Vas) does not seem to be required in mucosal head and neck squamous cell carcinoma. It should be considered only in cases of skin cancer of the posterior scalp and posterior neck. Level V receives efferent lymphatics from the occipital and postauricular nodes and from the occipital and parietal scalp, skin of the lateral and posterior neck and shoulder, nasopharynx, and oropharynx (tonsils and base of the tongue). Level V lymph nodes are at high risk for harboring metastases from cancers of the nasopharynx and oropharynx. Nodes in level Va are more often associated with primary cancers of the nasopharynx, oropharynx, or cutaneous structures of the posterior scalp, whereas those in level Vb are more commonly associated with tumors arising in the thyroid gland.

Level VI lymph nodes, also called the anterior compartment group, are the nodes located in the visceral space: the pretracheal and paratracheal nodes, precricoid (Delphian) node, and perithyroid nodes, including the lymph nodes along the recurrent laryngeal nerves. Level VI is limited cranially by the hyoid bone, caudally by the suprasternal notch, and laterally by the medial border of both carotid sheaths. Level VI receives efferent lymphatics from the thyroid gland, glottic and subglottic larynx, hypopharynx, and cervical esophagus. These nodes are at high risk for harboring metastases from cancers of the thyroid gland, glottic and subglottic larynx, apex of the piriform sinus, and cervical esophagus.

Imaging of the Neck

The armamentarium available for the imaging workup of the metastatic cervical lymph nodes includes computed tomography (CT), magnetic resonance imaging (MRI), ultrasonography, and positron emission tomography (PET).¹⁰ Nodal imaging is mandatory in a pretreatment workup because clinical assessment of the nodal status in patients with a thick and/or small neck has a low sensitivity and because deeply located nodes remain inaccessible in all patients.¹¹

CT and MRI are standard cross-sectional imaging modalities through which anatomic “slices” of the entire neck depict the contours and internal structure of the nodes (Figs. 38-2 and 38-3). MRI may have an advantage over CT scanning because of the higher spontaneous contrast it reveals between fatty and nonfatty tissues. The multiplanar capability of MRI has been an advantage of this technique since its introduction into clinical use in the early 1980s. However, the multirow detector technology and the spiral acquisition modality of newer-generation CT systems have boosted the multiplanar reformatting capabilities of CT scans, which now equal those of MR images. The major criteria for nodal malignancy using CT and/or MRI include the size of the nodes (a short axis longer than 10 mm) and the presence of a central necrosis (hypodensity on CT images; hypointensity on T1-weighted MR images and hyperintensity on T2-weighted MR images). Central necrosis is well highlighted by intravenous contrast agent perfusion, which enhances nodal areas with arterial blood supply on both CT and MR images (see Figs. 38-2A and 38-3C). However, the two techniques share common weaknesses: the inability to detect micrometastatic deposits within normal-sized nodes (false-negative results) and the risk for inappropriate classification of malignancy in nodes that are enlarged by benign reactive changes (false-positive results). Thus far, neither MRI nor CT can provide perfect diagnostic accuracy for nodal metastatic workup. It has been shown in a large series of patients that the two techniques have an almost similar and unsatisfactory performance.¹²

Figure 38-2 CT nodal display in a patient with left oropharyngeal squamous cell carcinoma (SCC). A, Native contrast-enhanced slice in the axial transverse plane using multislice multirow detector (MSMD) spiral acquisition technique. Hypodense fatty (F) environment allows clear delineation of the neck structures. Left oropharyngeal SCC (PT) is present. Abnormal nodes are seen within the left level II region, with anterior adenomegaly (long axis of 26 mm is shown as dotted line; short transverse axis of 18 mm is shown between the double-ended arrow) and a posterior, normal-sized node showing necrotic hypodensity (thick arrow). Normal-sized contralateral nodes are indicated (thin arrows). Observe the isodensity of the submandibular glands (ball-arrowhead) and of the muscles (double ball-arrowhead). Jugular veins (J) and carotid arteries (C) are strongly opacified at this early second phase of biphasic iodinated contrast agent perfusion. Notice the lamination of the left internal jugular vein by adenomegaly. B, Reformatted image in the coronal plane from the same three-dimensional data set shows the primary tumor (PT), left metastatic adenomegaly, and contralateral, normal-sized nodes (ball-arrowhead). Observe the irregularities of the inferior aspect of the enlarged node, suggesting extranodal spread (thin arrow) and hypodense foci corresponding to necrotic areas within adenomegaly (thick arrow).

Courtesy E. Coche, MD, PhD.

Figure 38-3 Magnetic resonance nodal display in a patient with right oropharyngeal squamous cell carcinoma (SCC). A, Transverse, unenhanced, T1-weighted spin-echo (SE) image showing a left level II hypointense necrotic adenomegaly (arrow) with a normal contralateral node in level II (ball-arrowhead). B, Transverse, T2-weighted fast spin-echo (FSE) image with fat suppression option in a similar slice location discloses strong hyperintensity of the necrotic node due to fluid-like content (arrow) compared with the normal contralateral node, which displays the usual intermediate to high signal intensity (ball-arrowhead). Observe the almost similar signal intensity of the normal node and of the parotid and submandibular glands (thin arrows). C, Transverse, contrast-enhanced, T1-weighted SE image with fat suppression option in a similar slice location as in A and B shows only peripheral ring-like enhancement of the margin of the necrotic adenomegaly (arrow). The normal contralateral node enhances slightly and homogeneously (ball-arrowhead). D, Coronal-view, precontrast, T1-weighted MR image shows a primary tumor (PT) and hypointense necrotic adenomegaly (arrow).

Ultrasonography has long been regarded as a low-cost, widely available, and innocuous alternative to CT/MRI, with the additional advantages of color Doppler flow–encoded vascular architecture depiction and fine-needle aspiration guidance. However, time demands and operator skill requirements are limiting factors, as well as the unresolved technical difficulties of fusing two-dimensional ultrasound data and three-dimensional CT/MRI data for radiotherapy planning. Ultrasound is also less efficient than CT and MRI at detecting nodal necrosis,¹³ and deeply located nodes may be poorly accessible to the technique.

Research is underway to improve the diagnostic accuracy of MRI, including experimental lymphophilic contrast agents, magnetization transfer imaging (MTI), free water diffusion-weighted imaging (DWI), magnetic resonance spectroscopy (MRS), and bolus tracking perfusion-weighted imaging (PWI).^14–16 Currently, only the DWI MR technique has made a definite breakthrough in clinical routine by yielding fast-to-acquire and easy-to-process accurate quantitative data that significantly add to pretherapeutic nodal staging attempts,^17–19 early prediction of therapeutic response,²⁰ and post-treatment early detection of residual/recurrent tumor.²¹ Many think that molecular imaging probes targeting either specific membrane antigens or metabolic pathways of tumor cells could be the definitive contributors to perfect diagnostic accuracy in nodal metastatic workup, in which case MRI and PET will be competitors.

PET using fluorodeoxyglucose (FDG) as a tracer has become the most available technique for “metabolic imaging” by enhancing foci of increased glucose uptake. However, PET alone provides only restricted diagnostic accuracy. The limitations of PET can be offset by coregistering the information on anatomic CT or MR images²² (Fig. 38-4). Integrated PET/CT combines the poor anatomic localization of PET with the accurate morphologic data provided by CT. The results of a recent large, prospective study showed that FDG-PET significantly improved the staging of HNSCC because of its detection of metastatic or additional disease.²³ However, a recent meta-analysis totaling 1236 patients demonstrated that the accuracy of FDG-PET was only marginally superior to that of CT or MRI; this study calls into question the routine value of FDG-PET for nodal staging.²⁴ In addition to research on dedicated tissue-specific MR contrast agents, research is under way on PET radiopharmaceutical tracers that would allow the assessment of hypoxia, angiogenesis, apoptosis, and receptor status; these studies make up the second main field of research in oncology imaging.²⁵ Using anatomic imaging studies to detect tumor recurrences in previously treated primary sites is unsatisfactory because extensive unspecific post-therapeutic changes may mask small foci of neoplastic recurrence.²⁶ On the other hand, very promising data have been reported with the use of FDG-PET in this setting.²⁷ Similar concepts apply to nodal metastases, and it may be possible that molecular and metabolic imaging methods will also become standard in nodal relapse detection. The key imaging concept for the radiation oncologist’s day-to-day practice is the capability of superimposing PET/MRI metabolic/molecular mapping onto CT/MRI anatomic images to improve the delineation of the irradiation target.²⁸ PET-CT and PET-MRI fusions are the founding paradigms that have now emerged into the clinical routine²⁹ (see Figs. 38-3 and 38-4).

Figure 38-4 CT-MRI-PET image fusion. A, Postcontrast, reformatted CT image in the coronal plane shows bilateral, mildly enlarged metastatic nodes in the carotid-jugular chains. Tumoral involvement of the nodes remains speculative because of the borderline short-axis diameter and absence of obvious necrotic changes. B, Superimposition of ¹⁸F-fluorodeoxyglucose positron emission tomography (FDG-PET) data on a CT image demonstrates increased glucose uptake within the nodes. C, Postcontrast, T1-weighted, axial transverse MR image from three-dimensional gradient-echo acquisition using spoiled gradients (SPGR) shows bilateral anterior, horseshoe-sized oropharyngeal tumor and metastatic left-sided nodes in level II. D, Superimposition of FDG-PET data on an MR image demonstrates increased glucose uptake within the primary tumor and metastatic nodes.

Courtesy M. Lonneux, MD, PhD.

Staging of Neck Node Metastases

The seventh edition (2009) of the American Joint Committee on Cancer (AJCC) staging for neck node metastases³⁰ is presented in Table 38-2. This classification does not apply to nasopharyngeal, thyroid, or skin cancers. The classification for nodal staging applies whether the modality used for neck assessment is clinical examination or imaging. The routine use of CT or MRI and—in expert hands—ultrasound is recommended especially for assessing nodes not clinically identifiable (e.g., retropharyngeal, intraparotid, or superior mediastinal nodes) or for patients for whom clinical palpation of the neck is less sensitive (e.g., those who have a thick or small neck).³¹ Last, it should be emphasized that the Nx classification applies only when the neck has not been assessed or could not be assessed.

TABLE 38-2 American Joint Committee on Cancer Staging for Neck Node Metastasis

Incidence and Distribution of Neck Node Metastases

Clinical and Radiologic Assessment

The metastatic spread of head and neck tumors into the cervical lymph nodes is rather consistent and follows predictable pathways, at least in the neck that has not been violated by previous surgery or radiotherapy. In Table 38-3, the frequency of metastatic lymph nodes is expressed as a percentage of node-positive patients.^32,33

TABLE 38-3 Distribution of Clinical Metastatic Neck Nodes from Oral Cavity and Pharyngolaryngeal Squamous Cell Carcinomas

The frequency of neck node metastases and the distribution of clinically involved nodes depend to a major extent on the primary tumor site. Typically, hypopharyngeal tumors have the highest propensity for nodal involvement, which occurs in 70% of cases. Cranial and anterior tumors (e.g., oral cavity tumors) mainly drain into levels I, II, and III, whereas more caudally located tumors (e.g., laryngeal tumors) mainly drain into levels II and III and, to a lesser extent, levels IV and V. Contralateral nodes are rarely involved except for midline tumors or tumors in sites where bilateral lymphatic drainage has been reported, such as the soft palate, base of the tongue, and pharyngeal wall. Even in these tumors, the incidence of contralateral involvement is much lower—in base of the tongue tumors with clinically positive nodes, the rate is 31% in the contralateral level II nodes compared with 73% in the ipsilateral level II nodes (data not shown). Node distribution follows the same pattern in the contralateral neck as in the ipsilateral neck. Except for nasopharyngeal tumors, involvement of ipsilateral level V nodes is rather rare, occurring in less than 1% of oral cavity tumors, in less than 10% of oropharyngeal and laryngeal tumors, and in about 15% of hypopharyngeal tumors. It almost never occurs in contralateral level V nodes.

Metastatic lymph node involvement in the neck depends on the size of the primary tumor, increasing with the T category. In the series reported by Bataini and associates,³² 44% of patients with a T1 tumor had clinical lymph node involvement; this increased to 70% for patients with T4 lesions. There are, however, no data suggesting that the relative distribution of involved neck levels varies with the T category.

Retropharyngeal lymph nodes represent a special entity because they are usually not clinically detectable. The incidence of retropharyngeal lymph node involvement can be estimated only from series in which CT or MRI of the retropharynx has been systematically performed as part of the diagnostic procedure. Retropharyngeal node involvement occurs in primary tumors arising from (or invading) the mucosa of the occipital and cervical somites, such as the nasopharynx, pharyngeal wall, and soft palate (Table 38-4). The incidence of retropharyngeal lymph node involvement is higher in patients in whom involvement of other neck node levels has also been documented. However, in patients with clinical stage N0 nasopharyngeal tumors and, to a lesser extent, in patients with pharyngeal wall tumors, the incidence of retropharyngeal node involvement is still significant—between 16% and 40%. Also, as already described for the other lymph node levels, involvement depends on the T category and is typically lower for T1 tumors. Accurate figures are not available.

TABLE 38-4 Incidence of Retropharyngeal Lymph Nodes in Oral Cavity and Pharyngolaryngeal Primary Tumors

Pathologic Lymph Node Metastases

The distribution of pathologic lymph node metastasis in patients with primary tumors of the oral cavity, oropharynx, hypopharynx, and larynx can be derived from retrospective series in which a systematic radical neck node dissection was proposed as part of the initial treatment procedures.^34–37 Retrospective series are essentially biased regarding patient and treatment selection, but these series from the Head and Neck Department at MSKCC are the largest and most consistent data ever published on that matter. The results of these retrospective studies are shown in Tables 38-5 to 38-8. The data are presented in terms of the number of neck dissections with positive lymph nodes divided by the total number of neck dissection procedures and expressed as a percentage. Most patients (>99% for patients with N0 tumors and 95% for patients with N+ tumors) had unilateral treatment only, and no distinction between the ipsilateral and contralateral neck was made.

TABLE 38-5 Incidence of Pathologic Lymph Node Metastasis in Squamous Cell Carcinomas of the Oral Cavity

TABLE 38-6 Incidence of Pathologic Lymph Node Metastasis in Squamous Cell Carcinomas of the Oropharynx

TABLE 38-7 Incidence of Pathologic Lymph Node Metastasis in Squamous Cell Carcinomas of the Hypopharynx

TABLE 38-8 Incidence of Pathologic Lymph Node Metastasis in Squamous Cell Carcinomas of the Larynx

Overall, metastatic disease was detected in 33% of the prophylactic neck dissections and in 82% of the therapeutic neck dissections. In these series, the overall sensitivity and specificity of the clinical examination reached 85% and 62%, respectively. As already observed with the pattern of clinical metastatic lymph nodes, the distribution of pathologically confirmed metastatic lymph nodes depended on the primary tumor site. Typically, in patients with clinical stage N0 oral cavity tumors, metastatic lymph nodes were observed in levels I to III, and in patients with clinical stage N0 oropharyngeal, hypopharyngeal, and laryngeal tumors, in levels II to IV. This pattern of node distribution is similar to that determined from the clinical palpation of the neck. It should be noted that the T-category distribution was different in the various groups. Of patients with laryngeal tumors, 54% (42 of 79) had stage T3 to T4 tumors (mainly, supraglottic lesions) compared with 27% of patients with oral cavity tumors (52 of 192), 25% of patients with hypopharyngeal tumors (6 of 24), and 17% of patients with oropharyngeal tumors (8 of 47). Such a difference in T category presumably explains the high incidence of microscopic node metastases in the group with laryngeal tumors.

The pattern of metastatic node distribution in patients who underwent therapeutic neck dissection was similar to that observed in patients with N0 tumors, with the difference that significant pathologic infiltration of an additional nodal level was typically observed—level IV for oral cavity tumors and levels I and V for oropharyngeal, hypopharyngeal and, to a lesser extent, laryngeal tumors. Overall, this observation illustrates the gradual infiltration of node levels in the neck. This concept is well illustrated by the prevalence of metastases in level V. In the MSKCC series,³⁸ the prevalence of pathologic infiltration in level V was quite low, averaging 3% in 1277 neck dissections in patients with oral cavity, oropharyngeal, hypopharyngeal, and laryngeal tumors. The prevalence peaked at 11% for hypopharyngeal tumors with pathologically positive nodes (see Table 38-7). A thorough analysis of level V infiltration showed that for all tumor sites pooled together, infiltration of level V without metastases in levels I to IV was observed in only one patient (0.2%). This patient had a hypopharyngeal tumor. Infiltration in level V remained below 1% when a single pathologically confirmed positive node was also observed in levels I to III, but reached 16% when a single pathologically confirmed positive node was also observed in level IV. When more than one level was infiltrated, the probability of level V involvement progressively increased, reaching 40% when levels I to IV were all involved. The pattern of involvement of level I is also a good illustration of the concept of gradual node infiltration. In the MSKCC series, pathologic involvement of level I was found in only 2% of patients with clinical stage N0 oropharyngeal tumors (see Table 38-6) and was not observed in patients with clinical stage N0 hypopharyngeal tumors (see Table 38-7). On the other hand, in patients with clinically positive nodes, metastases in level I were reported in 15% and 10% of patients with oropharyngeal and hypopharyngeal tumors, respectively.

Recommendations for Selection of Target Volumes in the Neck

Metastatic lymph node involvement of primary squamous cell carcinoma of the oral cavity, pharynx, and larynx typically follows a predictive pattern. Data on clinical and pathologic neck node distribution as well as on neck recurrence after selective dissection procedures support the concept that not all neck node levels should be treated as part of the initial management strategy of head and neck primaries of squamous cell origin.^45,46 However, the data on which such a concept is based have come from retrospective series and so may include possible biases (e.g., in patient selection, use of a series from the preimaging area, and so on) that could limit their validity.

Tables 38-9 to 38-12 present recommendations for the selection of clinical target volumes in the neck for pharyngolaryngeal squamous cell carcinomas. These guidelines can be applied whether the treatment modality is surgery or radiotherapy. A complete discussion on choosing between these two modalities is beyond the scope of this chapter, but factors to consider include the neck stage, the treatment option for the primary tumor, the performance status of the patient, and the institutional policy agreed on by a multidisciplinary head and neck tumor board.

TABLE 38-9 Recommendations for Selection of Clinical Target Volume in the Neck for Oral Cavity Tumors

* Level IIb could be omitted for stage N0 tumors.

† For anterior tongue tumor and any tumor with extension to the oropharynx (e.g., anterior tonsillar pillar, tonsillar fossae, base of tongue).

‡ Level V could be omitted if only levels I to III are involved.

TABLE 38-10 Recommendations for Selection of Clinical Target Volume in the Neck for Oropharyngeal Tumors

* Any tumor with extension to the oral cavity (e.g., retromolar trigone, mobile tongue, inferior gum, oral side of anterior tonsillar pillar).

TABLE 38-11 Recommendations for Selection of Clinical Target Volume in the Neck for Hypopharyngeal Tumors

* Level IIb could be omitted for stage N0 tumors.

TABLE 38-12 Recommendations for Selection of Clinical Target Volume in the Neck for Laryngeal Tumors (Stage T1 N0 Glottic Carcinoma Excluded)

* Level IIb could be omitted for stage N0 tumors.

Selective treatment of the neck is appropriate for patients with clinical N0 HNSCC of the oral cavity, oropharynx, hypopharynx, and larynx.39,46,47 Typically, level I to III nodes should be treated for oral cavity tumors, and level II to IV nodes should be treated for oropharyngeal, hypopharyngeal, and laryngeal tumors. Robbins⁷ suggested that elective treatment of level IIb nodes is probably not necessary for patients with clinical stage N0 primary tumors of the oral cavity, larynx, or hypopharynx. However, Byers and associates⁴⁰ suggested that level IV nodes be included in the treatment of the mobile tongue because of the high incidence (10%) of skip metastases. Retropharyngeal nodes should be treated in tumors of the posterior pharyngeal wall. For subglottic tumors, tumors with subglottic or transglottic extension, or hypopharyngeal tumors with esophageal extension, level VI nodes should also be included in the treatment volume.

As proposed by Byers,⁴⁷ similar guidelines could be recommended for patients who have N1 tumors without radiologic evidence of extracapsular infiltration. However, when an involved lymph node is located at a boundary of a level that has not been selected for the target volume, it is recommended to extend the selection to include the adjacent level.⁴⁸ Typically, this applies only for oropharyngeal tumors with a single lymph node involved in level II at the boundary with level Ib or for an oral cavity tumor with an N1 node in level III at the boundary with level IV.

For patients with multiple nodes (N2b), the available data suggest that adequate treatment should include nodes in levels I to V. Level I nodes could, however, be omitted for laryngeal tumors, and level V nodes omitted for oral cavity tumors with neck involvement limited to levels I to III. Prophylactic treatment of the retropharyngeal nodes should be systematically performed for oropharyngeal and hypopharyngeal tumors. Patients with N0 disease should have level VI nodes treated for subglottic tumors, tumors with subglottic or transglottic extension, or hypopharyngeal tumors with esophageal extension. It has been proposed that patients with nodes in the upper neck (i.e., upper level II nodes) have the upper limit of the target volume extended to include the retrostyloid space.⁴⁸ Similarly, the subclavicular fossae should be included in the target volume in cases of lower neck involvement (i.e., level IV or Vb nodes).⁴⁸

There are no data available on the distribution of pathologic metastatic neck nodes in patients presenting with a single ipsilateral large node (N2a or N3) or with bilateral or contralateral nodes (N2c). For patients with a single large node—in the absence of data—it appears safe not to recommend selective treatment. For N3 disease, the type of treatment of the neck is also likely to be dictated by the local extension of the node into the adjacent structures (e.g., paraspinal muscles, parotid gland, blood vessels). For N2c tumors, one proposal is to consider each side of the neck separately, such as selective treatment on both sides for a small single node on each side, selective treatment for a small single node on one side, and more extensive treatment on the other side in the case of multiple nodes.

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