Management of Cervical Metastasis

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PETER E. ANDERSEN, MD, FACS SCOTT SAFFOLD, MD

Head and neck cancer represents less than 5 percent of all cancers in the United States and will be responsible for approximately 11,800 deaths in 2001.1 However, worldwide it ranks as the sixth most common cancer,2 thus making head and neck cancer a major health problem. While the term "head and neck cancer" refers to tumors of myriad sites of origin and histologic types, over 90 percent of these are squamous carcinomas arising from the epithelium of the upper aerodigestive tract (oral cavity, oropharynx, hypopharynx and larynx) and for the purposes of this discussion the term shall refer exclusively to these tumors.

The status of the regional lymphatics is one of the most important prognostic indicators in patients with head and neck cancer. Head and neck cancers that are localized to the primary site without regional lymph node metastasis have excellent cure rates with either surgery or radiation therapy. The presence of regional metastases results in cure rates that are approximately half of those obtainable if metastasis to the regional lymphatics is not present. Thus the treatment of the neck has become one of the most actively debated topics in the field of head and neck oncology. Treatment of the neck in patients with clinical evidence of nodal metastasis has traditionally been surgical. In recent decades this has been extended to include a combination of surgery and radiation therapy. The role of chemotherapy in the management of neck disease remains controversial and is currently being actively investigated.

Butlin3 was the first surgeon to systematically address the cervical lymph nodes by excising the nodal tissue of the submandibular triangle in continuity with the primary lesion in patients with cancer of the tongue. This did not remove all of the lymphatic tissue in the neck that was at risk for metastasis and it was not until the radical neck dissection (RND) described by Crile4 and later popularized by Martin5,6 that systematic removal of all of the lymphatic tissue in the lateral neck became routine.

Radical neck dissection, however, is cosmetically deforming and produces a characteristic shoulder disability that has been termed the "shoulder syndrome."7 In an effort to lessen the morbidity of classic RND, various modifications have been proposed that preserve non-lymphatic structures that are normally sacrificed during this procedure but still remove all of the nodal tissue excised in RND. These modifications in general include preservation of the spinal accessory nerve (SAN) and can also involve preservation of the internal jugular vein (IJV) and/or the sternocleidomastoid muscle (SCM). More recently, further modifications of neck dissection have been proposed which preserve all of the non-lymphatic structures removed in "then-RND" but do not remove all of the lymphatic tissue on the involved side of the neck. These operations, which have been termed selective neck dissections, are based on observations that cancers of the head and neck tend to metastasize in predictable patterns based on the location of the primary tumor. Whether these modifications avoid all of the morbidity of RND is ambiguous, however there is evidence that shoulder function is retained when the spiral accessory nerve is preserved.8,9,10

Anatomy of Cervical Lymphatics

The lymphatics of the head and neck are a rich plexus of vessels whose anatomy was described by Rouviere and others.11,12 There are many methods of clinically describing locations of lymph nodes; however the method that is in widest use and most reproducible is the system described by the Head and Neck Service at Memorial Sloan-Kettering Cancer Center. This system divides the neck into 5 nodal groups or levels, which are described in Figure 15-1.13

Classification of Neck Dissections

With the development of the many modifications of the classic RND there has been a proliferation of terms to describe these various procedures. This has resulted in a nomenclature that is non-uniform and confusing. To facilitate communication and to ensure standardization, the American Academy of Otolaryn-gology, Head and Neck Surgery has proposed a classification scheme for neck dissection.13 In this scheme, RND, which is defined as the removal of nodal groups I to V with the SCM, IJV, and SAN, is considered to be the standard basic neck dissection, while all other procedures are considered to be modifications of RND. Modified radical neck dissection (MRND) consists of preservation of one or more of the non-lymphatic structures normally removed in RND. Selective neck dissection consists of removal of one or more regional lymph node groups with preservation of the SAN, SCM, and IJV This nomenclature is described in greater detail in Table 15-1 and Figure 15-2. The typical postoperative appearance of patients after various neck dissections are shown in Figure 15-3, Figure 15-4, Figure 15-5, and Figure 15-6. The routine use of a standardized system will greatly reduce the confusing nomenclature currently used in describing neck dissections.

Patterns of Lymphatic Flow

The entire concept of selective or limited neck dissection is based on the clinical observation that

Metastasis Cervicales

Group

Description

Submental group-The nodal tissue lying between the anterior belly of the digastric muscles and above the hyoid bone. Submandibular group-Nodal tissue lying in the triangle bounded by the anterior and posterior bellies of the digastric muscle and the inferior border of the mandible.

Upper jugular group-Nodal tissue lying around the upper portion of the LTV and the upper SAN. Extending from the skull base to the bifurcation of the carotid artery or the hyoid bone (clinical landmark), the posterior limit is the posterior border of the SCM and the anterior border is the lateral border of the sternohyoid muscle.

Middle jugular group-Nodal tissue lying around the middle third of the DV from the inferior border of level 2 to the omohyoid muscle or the cricothyroid membrane (clinical landmark). The anterior and posterior borders are the same as those for level

Lower jugular group -Nodal tissue lying around the inferior third of the LTV from the inferior border of level 3 to the clavicle. The anterior and posterior borders are the same as those for level 2 and 3,

V Posterior triangle group-Nodal tissue around the lower portion

Figure 15-1. System for describing location of cervical lymphatic metastases. IJV = internal jugular vein; SAN = spinal accessory nerve; SCM = sternocleidomastoid.

Table 15-1. Classification of Neck Dissections

Nodal Levels

Structures

Type of Neck Dissection

Dissected

Preserved

Radical neck dissection (RND)

I-V

None

Type I modified radical

I-V

SAN

neck dissection (MRND I)

Type II modified radical

I-V

SAN

neck dissection (MRND II)

SCM

Type III modified radical

I-V

SCM

neck dissection (MRND III)

IJV

SAN

Supraomohyoid neck

I-III

SCM

dissection (SOHND)

IJV

SAN

Lateral (jugular) neck

II-IV

SCM

dissection (LND)

IJV

SAN

Anterolateral neck

I-IV

SCM

dissection (ALND)

IJV

SAN

Posterolateral neck

II-V

SCM

dissection (PLND)

IJV

SAN = spinal accessory nerve; SCM = sternocleidomastoid; IJV = internal jugular vein.

SAN = spinal accessory nerve; SCM = sternocleidomastoid; IJV = internal jugular vein.

squamous cell carcinomas of the upper aerodiges-tive tract metastasize to the cervical lymph nodes in a predictable pattern. Strong experimental evidence of this concept's validity is provided by Fisch,14 who performed lymphography using oil-based contrast media injected into postauricular lymphatics. Twenty-four hours after injection the patients underwent complete neck dissection and filling of the lymph nodes was verified in almost every one of his 100 cases. The flow of the contrast material was observed with radiography. From observations obtained from 8 cases that were free of lymph node metastases, Fisch was able to document the normal pattern of flow in the cervical lymphatics.

After injection in the postauricular lymphatics, contrast first flowed into a group of nodes just below and behind the angle of the mandible. These nodes were called the junctional nodes by Fisch and probably represent either high level V or high level II nodes. From the junctional nodes, contrast

Postauricular Injection
Figure 15-2. Cervical lymph node groups removed in various types of neck dissection.

Figure 15-3. Cosmetic and functional deformity resulting from radical neck dissection. A, Anterior view demonstrating anterior and inferior displacement of shoulder and trapezius muscle (arrow). B, Anterior view demonstrating decreased shoulder abduction. C and D, Posterior view demonstrating winging of scapula. (Photos courtesy of James I. Cohen, MD, PhD.)

Figure 15-3. Cosmetic and functional deformity resulting from radical neck dissection. A, Anterior view demonstrating anterior and inferior displacement of shoulder and trapezius muscle (arrow). B, Anterior view demonstrating decreased shoulder abduction. C and D, Posterior view demonstrating winging of scapula. (Photos courtesy of James I. Cohen, MD, PhD.)

flowed first into both the lymphatics along the spinal accessory nerve and the internal jugular vein. Contrast in the lymphatics along the spinal accessory nerve then flowed into the transverse cervical chain, and through this medially into the low jugular chain. Of particular interest is the observation that contrast contained within the lymphatics of the spinal accessory chain could reach the jugular chain lymphatics by connecting vessels which occurred at many places along the spinal accessory chain. Contrast contained within the jugular chain could not, however, reach the spinal accessory chain by retrograde flow along the same route. Flow to contralateral lymphatics or retrograde lymphatic flow was not observed. These patterns are shown in Figure 15-7. A critical question left unanswered by the studies of Fisch is the precise location of the junctional nodes he described. If these nodes are commonly involved by head and neck cancer metastasis, it is possible virtually anywhere in the neck, and the concept of selective neck dissection would seem to be unsound. However, as will be shown in the section on patterns of nodal metastasis from squamous carcinomas of the upper aerodigestive tract, these junctional nodes are probably uninvolved in most cases of head and neck cancer since metastasis to level V is uncommon, except in nasopharyngeal carcinoma.

Lymphedema After Neck Dissection

Figure 15-5. Postoperative appearance of neck after supraomo-hyoid neck dissection.

Figure 15-4. Postoperative appearance of neck after modified radical neck dissection, type I.

Figure 15-5. Postoperative appearance of neck after supraomo-hyoid neck dissection.

Figure 15-6. Postoperative appearance of neck after bilateral modified radical neck dissections, type III.

Incidence and Pattern of Nodal Metastasis

The rational use of modifications of RND, especially selective neck dissection, is based upon work describing the patterns of lymphatic metastasis. These studies have shown that patterns of metastasis can be predicted based upon knowledge of the primary tumor location. Without such validation the concept of selective neck dissection would be invalid, since by definition nodal tissue at risk for metastasis would be left behind in the neck.

Lindberg published the location of nodal metastases in patients with squamous carcinoma of the upper aerodigestive tract as determined by clinical examination15 in 1972. This review consisted of 2,044 previously untreated patients with squamous carcinoma of the head and neck. The presence of nodal metastasis and their location was assessed and correlated with the location and stage of the primary site. Primary sites were divided into oral tongue, floor of mouth, retromolar trigone/anterior faucial pillar, soft palate, tonsillar fossa, base of tongue, oropharyngeal walls, supraglottic larynx, hypopharynx and nasopharynx. Fifty-seven percent of patients presented with clinical evidence of metastasis in the cervical nodes. Lindberg showed that for lesions of the oral tongue, floor of mouth, retromolar trigone/anterior faucial arch and soft palate, the incidence of cervical nodal metastasis increased with the size of the primary tumor. However, the incidence of nodal metastasis did not correlate with the size of the primary in tumors of the tonsillar fossa, base of tongue, supraglottic larynx, and hypopharynx.

Lindberg demonstrated that squamous cell carcinomas of the upper aerodigestive tract tend to metastasize to the neck in a predictable pattern. By far the most common site of metastasis by all tumors is to the ipsilateral level II nodes. Tumors that lie within the oral cavity anterior to the circum-vallate papillae have a propensity to metastasize to levels I through III, with levels IV and V seldom involved. Tumors of the oropharynx have a low propensity to metastasize to level I; metastasis is most common to level II with decreasing incidence of metastasis in levels III and IV These tumors have a higher rate of metastases to level V than oral cavity tumors but the rate is still low. Tumors of the supraglottic larynx and hypopharynx rarely metas-tasize to level I, again metastases were most com-

Cervical Lymphatic System
Figure 15-7. Pattern of lymphatic flow as demonstrated by Fisch. Data from Fisch UP, et al. Cervical lymphatic system as visualized by lymphography. Ann Otol Rhinol Laryngol 1964;73:869-82.

mon to level II with a decreasing incidence in levels III and IV and metastases to level V were infrequent. Tumors of the nasopharynx are unique among squamous cell carcinomas of the upper aerodigestive tract in that they metastasize widely to levels II through V Contralateral metastases were uncommon in cancers of the floor of mouth, oral tongue, hypopharynx, and retromolar trigone/ante-rior faucial arch. In contrast, tumors of the nasopharnyx, base of tongue, oropharyngeal walls, soft palate, supraglottic larynx, and tonsil have substantial rates of contralateral metastases.

Lindberg's data clearly showed that in cases of squamous cell carcinoma of the upper aerodigestive tract, with the exception of nasopharyngeal carcinoma, nodal metastasis occurs in a predictable pattern and it may, in certain instances, be sound to exclude dissection of the level V lymph nodes. However, this study provides only information on clinically positive nodal metastasis—it provides no information on the incidence and location of occult nodal metastasis. Such information on microscopic metastasis can only be obtained from a surgical specimen. Byers and colleagues published one such study16 in 1988. They examined the specimens of 428 patients undergoing 648 modified neck dissections and correlated the location of the pathologically positive lymph nodes with the primary site. The majority of these neck dissections were selective neck dissections and therefore not all of the lymph node levels at risk were examined in each patient. This study essentially confirms the clinical data of Lindberg,15 that lesions anterior to the circumvallate papillae are most likely to metastasize to lymph nodes levels I through III and lesions within the hypopharynx and larynx to levels II through IV. It must be pointed out, however, that the majority of these dissections were less than comprehensive and therefore the low incidence of metastasis to certain nodal levels may simply reflect the lack of sampling of those levels.

In order to fully assess all the lymph node levels at risk for a particular primary site, surgical specimens should include all lymph node levels (comprehensive neck dissection). Just such information is provided in a series of studies by Shah and col-leagues,171819 which involved 1,081 previously untreated patients who underwent 1,119 classic

RNDs for squamous carcinoma of the upper aerodi-gestive tract. The operations consisted of 343 elective RND in the clinically N0 setting and 776 therapeutic RND in the clinically N+ setting.

The results of Shah's studies are shown in Figure 15-8. Each lymph node level shows the percentage of patients with pathologically N+ neck dissections who had metastasis at that level. In patients with primary tumors of the oral cavity undergoing therapeutic RND, the majority of metastatic nodes were located in levels I to III; level IV was involved in 20 percent of specimens and level V in only 4 percent. In those with primary oropharyngeal tumors, the majority of metastases were located in levels II to IV; levels I and V were involved in 17 percent and 11 percent of the specimens respectively. Therapeutic neck dissection in hypopharyngeal tumors showed that the majority of metastases were located in levels II to IV, while levels I and V were involved in 10 percent and 11 percent of the specimens respectively. Primary tumors of the larynx metastasized to levels II through IV with levels I and V being involved in 8 percent and 5 percent of the specimens respectively.

In the setting of elective RND in patients with primary tumors of the oral cavity, the majority of metastases were located in levels I to III; levels IV and V were involved in 9 percent and 2 percent of the specimens respectively. In patients with primary tumors located in the oropharynx, the majority of metastases were located in levels II to IV; levels I and V were involved in 7 percent of the specimens each. Patients with tumors of the hypopharynx undergoing elective RND had the majority of metastases in levels II to IV, while levels I and V were not involved in any of the specimens. Primary tumors of the larynx metastasized primarily to levels II through IV, while levels I and V were involved in 14 percent and 7 percent of the specimens respectively.

The question of metastasis to level V was addressed by another study from Memorial Hospital by Davidson and colleagues.20 They examined the specimens of 1,123 patients undergoing 1,277 RNDs and found metastases to level V in only 3 percent of patients. Level V metastases were highest in patients with hypopharyngeal and oropharyngeal primary sites (7% and 6% respectively). Only 3 of the 40 patients with level V metastases had these in the face

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