Head and Neck Cancer: A Multidisciplinary Approach
2nd Edition

Chapter 13
Surgical Management of Cervical Lymph Nodes
Jesus E. Medine
John R. Houck, Jr.
Treatment of the regional lymph nodes is an integral component of the management of patients with squamous cell carcinoma (SCC) of the head and neck region. For several decades since the beginning of the 20th century, surgical treatment of cervical metastases consisted of radical neck dissection (RND) as described by Crile (1) in 1906 and popularized by Martin et al. (2) during the 1950s. During the last 20 years, significant changes have occurred in the treatment of the neck. As a result, today RND is not the only operation used for surgical treatment of the neck, and surgery is not the only treatment for every patient with cervical lymph node metastases (Fig. 13.1).
More than ever before, appropriate management of the cervical lymph nodes requires a good understanding of the incidence, patterns, and prognostic implications of lymph node metastases and of the role of combined surgery, radiation therapy, and chemotherapy in the treatment of the neck in cancer patients.
INCIDENCE OF CERVICAL METASTASES
The propensity of SCCs of the upper aerodigestive tract to metastasize to the cervical lymph nodes varies depending on the site of origin of the lesions and on the size of tumor or tumor (T) stage. Lindberg’s (3) classic incidence figures (based on the presence of palpable lymphadenopathy in more than 2,000 patients with SCC of the head and neck) have been refined by the studies of Byers et al. (4) and Shah (5), in which a large number of neck dissection specimens were evaluated (Tables 13.1,13.2). From these observations, we have learned that carcinomas of the pharynx have a higher propensity to metastasize to the lymph nodes than do carcinomas of the larynx and oral cavity. In fact, this propensity is so high for carcinomas of the nasopharynx, tonsillar fossa, base of the tongue, and hypopharynx that the rate of occurrence of lymph node metastases in patients with small (Tl and T2) and large (T3 and T4) tumors is between 70% and 90%. On the other hand, the incidence of lymph node metastases for T1 carcinomas of the oral cavity ranges only between 2% and 25%, but it increases as T stage increases.
PATTERNS OF SPREAD
Anatomic and radiographic studies of the lymphatics of the head and neck have demonstrated that the lymphatic drainage of the different areas of the upper aerodigestive tract occurs along predictable pathways (6,7). Furthermore, multiple clinical studies (5,8) have demonstrated that tumors from these areas metastasize to the lymph nodes following the same pathways, at least as long as the neck has not been treated previously with surgery or radiation therapy (Tables 13.3,13.4). A now commonly accepted concept is that the lymph node groups that harbor metastases most often in patients with carcinomas of the oral cavity are the submental (Ia), submandibular (Ib), upper jugular (II), and midjugular nodes (III), whereas in patients with tumors of the oropharynx, larynx, and hypopharynx, the lymph nodes along the jugular vein (II, III, and IV) are involved more frequently. These patterns of distribution have been shown convincingly to occur
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both in patients who are staged N0 clinically and are found to have occult metastases and in patients with palpable, histologically proved lymph node metastases (5,8). What must be kept in mind, however, is that skip metastases (i.e., direct metastases beyond the first or second echelon of expected lymphatic drainage) do occur (9).
Figure 13.1 Treatment of the neck. Squamous cell carcinoma of the upper aerodigestive tract. ECS, extracapsular spread; p, pathologic; RND, radical neck dissection.
TABLE 13.1 Incidence of Lymph Node Metastases
Site of primary tumor Percent of necks with nodal metastases
T1 T2 T3 T4
Oral cavity
   Oral tongue 14 30 47.5 76.5
   Floor of mouth 11 29 43.5 53.5
   Retromolar trigone 11.5 37.5 54 67.5
Oropharynx
   Tonsil 70.5 67.5 70 89.5
   Base of tongue 70 71 74.5 84.5
   Pharyngeal walls 25 30 67 76
Larynx
   Glottic
   Supraglottic 39 41.5 64.5 59
Hypopharynx 63 69.5 79 73.5
Nasopharynx 92.5 84.5 88.5 83
Data are based on physical examination.
Source: Modified from Lindberg R. Distribution of cervical lymph node metastases from squamous cell carcinoma of the upper respiratory and digestive tracts. Cancer 1972;29:1446–1449, with permission.
TABLE 13.2 Incidence of Histopathologic Lymph Node Metastases
Site of primary tumor T stage
T1-2 T3-4
Oral cavity
   Oral tongue 18.6 31.6
   Floor of mouth 18.6 26.3
   Lower gum 11.5 13.3
   Buccal mucosa
   Retromolar trigone 36.4 33.3
Oropharynx
   Tonsil
   Base of tongue 50.0
   Pharyngeal walls 20.0 62.5
Larynx
   Glottic 21.4 14.0
   Supraglottic 30.8 25.0
Hypopharynx
   Pyriform sinus 66.7 55.2
Source: Modified from Remmler D, Byers RM, Scheetz JE. A prospective study of shoulder disability resulting from radical and modified neck dissections. Head Neck Surg 1986;8:280–286, with permission.
TABLE 13.3 Pattern of Nodal Metastases
Primary site Percentage of nodal involvement
IA IB II III IV V
Oral tongue 3.3a 22.8 59.7 10.7 2.6 7.0
9.0b 18.0 73.0 18.0
c 14.0 19.0 16.0 3.0
Floor of mouth 4.3a 43.1 37.1 9.5 4.3 1.7
7.0b 64.0 43.0
c 16.0 12.0 7.0 2.0
Buccal mucosa a
b
c 44.0 11.0
Lower gum a
b 60.0 40.0
c 27.0 21.0 6.0 4.0 2.0
Retromolar trigone 0.6a 17.1 61.8 16.4 3.3 0.6
b 25.0 63.0 12.5
c 19.0 12.0 6.0 6.0 0.0
Supraglottic larynx 0.5a 1.0 47.6 34.0 10.7 6.3
b 48.0 38.0 5.0
c 6.0 18.0 18.0 9.0 1.5
Glottic larynx a
b 55.0 27.0
c 21.0 29.0 7.0 7.0
aBased on clinical examination (see ref. 3).
bBased on examination of selective neck dissections (see ref. 4).
cBased on examination of radical neck dissections (see ref. 5).
The retropharyngeal nodes must be emphasized as a common site for metastases in tumors of the hypopharynx, tonsillar fossa, soft palate, posterior and lateral oropharyngeal walls, and paratracheal nodes a common site of metastases for laryngeal carcinomas involving the subglottic region and for carcinomas of the cervical esophagus (10,11,12).
TABLE 13.4 Pattern of Nodal Metastases
Primary site Percentage of nodal involvement
IA IB II III IV V
Tonsil 0.6a 9.2 59.5 14.4 8.1 8.1
b
c
Base of tongue 0.8a 4.4 56.4 25.3 5.8 7.1
b 67.0 33.0 33.0 17.0
c
Pharyngeal wall 1.5a 3.6 56.9 22.6 5.10 10.2
b 20.0 80.0 40.0 40.0
c
Hypopharynx 0.3a 0.6 44.2 33.4 12.8 8.6
b 67.0 33.0 7.0
c 13.0 13.0
Nasopharynx 1.1a 2.6 44.8 16.8 8.6 26.1
b
c
aBased on clinical examination (see ref. 3).
bBased on examination of selective neck dissections (see ref. 4).
cBased on examination of radical neck dissections (see ref. 5).
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PROGNOSTIC IMPLICATIONS OF NECK NODE METASTASES
The presence of clinically obvious, histologically proven lymph node metastasis is the single most important prognostic factor in patients with SCC of the head and neck. In general, it decreases the overall survival by at least one-half (13). However, the unfavorable impact on survival varies, depending on certain factors.
The presence of extracapsular spread (ECS) of tumor has been explored in numerous studies that demonstrated that tumor extension beyond the capsule of a lymph node worsens the prognosis. Johnson et al. (14) report that less than 40% of patients with histologic evidence of ECS were free of disease 24 months after therapy. Furthermore, the survival of these patients was significantly lower than that in comparable patients whose metastases were confined to the lymph nodes (15). Similarly, Steinhart et al. (16) found that the rate of ECS was especially high (70%) in patients with carcinomas of the hypopharynx and that the 5-year survival rate differed greatly for patients with ECS of tumor (28%) and patients with no metastases (77%). Interestingly, a correlation between the degree of ECS and prognosis has not yet been established clearly, though Carter et al. (17) have reported that macroscopically recognizable ECS carries a prognosis worse than that of microscopic spread.
In a study performed at the Mayo Clinic, a desmoplastic stromal pattern in the lymph nodes involved by tumor was associated with an almost sevenfold increase in the risk for recurrence in the neck. The study included 284 patients who had pathologically confirmed metastatic SCC, underwent neck dissection, and did not receive adjuvant therapy (18). This finding has not been reported previously.
The number of lymph nodes involved affects the survival of patients with histologically positive nodes; survival is significantly lower when multiple nodes are involved (13). A study by Leemans et al. (19) reports a 10.7% overall incidence of distant metastases in a group of 281 head and neck cancer patients who underwent a neck dissection, whereas it was 46.8% in the group of patients with three or more positive nodes.
The level of the neck metastases figures significantly. Several studies have suggested that survival decreases as lymph nodes in lower levels of the neck become involved (20,21,22,23). This tendency has been demonstrated best by Ho (24) and Teo et al. (25) for nasopharyngeal carcinoma: the lower the level, the worse the prognosis. Grandi et al. (26) have defined three levels in the neck (upper, middle, and lower), divided by two imaginary lines that pass through the hyoid bone and through the lower border of the thyroid cartilage. They found that the worst prognosis was associated with the presence of nodal metastases at the lower level. On the basis of these observations, a new staging system has been adopted for the neck in patients with nasopharyngeal carcinoma (26, 27).
The prognostic significance of nonpalpable (occult) metastases in the N0 neck is less clearly defined. Studying it is more difficult because the T stage also affects prognosis and may overshadow the effect of occult neck nodes (28). However, ECS has been shown to occur in nonpalpable lymph nodes (4). Also, as in patients with palpable nodal metastases, the number and location of involved nodes in the N0 neck appears to affect prognosis (21,29,30,31). For instance, Kalnins et al. (32) found that patients with SCC of the oral cavity and uninvolved neck nodes had a 75% 5-year survival. Survival decreased to 49% when one node was histopathologically involved, to 30% when two nodes were involved, and to 13% when three or more nodes were involved by tumor.
TYPES OF NECK DISSECTION
The six levels currently used encompass the complete topographic anatomy of the neck. Lymph nodes involving regions not located within these levels should be referred to by the name of their specific nodal group; examples of these are the superior mediastinum, the retropharyngeal, the periparotid, the buccinator, the postauricular, and the suboccipital lymph nodes. The concept of sublevels has been introduced into the classification since certain zones have been identified within the six levels, which may have significance. These are sublevels IA (submental nodes), IB (submandibular nodes), IIA and IIB (together comprising the upper jugular nodes), and VA (spinal accessory nodes) and VB (transverse cervical and supraclavicular nodes). The boundaries for each of these sublevels are defined in Table 13.5, and are visually demonstrated inFigure 13.2.
The definitions of types of neck dissection recently proposed by the American Head and Neck Society and the American Academy of Otolaryngology Head and Neck Surgery remain unchanged as previously outlined in the 1991 classification report (32a). These are:
  • Radical neck dissection is considered to be the standard basic procedure for cervical lymphadenectomy. All other neck dissections represent one or more alterations of this procedure.
  • The operation is called modified radical neck dissection when the alteration involves preservation of one or more nonlymphatic structures routinely removed in the radical neck dissection.
  • The operation is called selective neck dissection when the alteration involves preservation of one or more lymph node groups/levels routinely removed in the radical neck dissection.
  • The operation is called extended neck dissection when the alteration involves removal of additional lymph node groups or nonlymphatic structures relative to the radical neck dissection.
The proposed new classification is essentially the same as the 1991 version with the exception that specific names for certain types of selective neck dissection should be de-emphasized. The rationale for this recommendation is based on the increased number of variations, which have been introduced over the past decade. A comparison of the two classifications is shown in Table 13.6.
Radical Dissection
Radical neck dissection consists of the removal of all five lymph node groups on one side of the neck, including the sternocleidomastoid muscle (SCM), the internal jugular vein (IJV), and the spinal accessory nerve (Fig. 13.3).
Modified Dissections
Modifications of RND were developed with the intention of reducing the morbidity of this operation by preserving one or more of the following structures: the spinal accessory nerve, the IJV, or the SCM. Like RND, the modified RNDs remove all five nodal groups on one side of the neck. The three neck dissections that can be included in this category differ from one another
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only in the number of neural, vascular, and muscular structures that are preserved. Therefore, Medina (33) suggests subclassifying these neck dissections (Table 13.7) as follows:
  • type I, in which only one structure the spinal accessory nerve is preserved (Fig. 13.4)
  • type II, in which two structures the spinal accessory nerve and the IJV are preserved (Fig. 13.5)
  • type III, in which all three structures the spinal accessory nerve, the IJV, and the SCM are preserved (Fig. 13.6).
TABLE 13.5 Lymph Node Levels and Sublevels
Lymph node level Description
Level 1 Sublevel IA (Submental): Lymph nodes within the triangular boundary of the anterior belly of the digastric muscles and the hyoid bone.
Sublevel IB (Submandibular): Lymph nodes within the boundaries of the anterior belly of the digastric muscle, the stylohyoid muscle, and the body of the mandible.
Level II (upper jugular) Lymph nodes located around the upper third of the internal jugular vein and adjacent spinal accessory nerve extending from the level of the skull base (above) to the level of the inferior border of the hyoid bone (below). The anterior (medial) boundary is the stylohyoid muscle (the radiologic correlate is the vertical plane defined by the posterior surface of the submandibular gland) and the posterior (lateral) boundary is the posterior border of the sternocleidomastoid muscle.
Sublevel IIA: Nodes located anterior (medial) to th evertical plane defined by the spinal accessory nerve.
Sublevel IIB: Nodes located posterior (lateral) to the vertical plane defined by the spinal accessory nerve.
Level III (midjugular) Lymph nodes located around the middle third of the nternal jugular vein extending from the inferior border of the hyoid bone (above) to the inferior border of the cricoid cartilage (below). The anterior (medial) boundary is the lateral border of the sternohyoid muscle, and the posterior (lateral) boundary is the posterior border of the sternocleidomastoid muscle.
Level IV (lower jugular) Lymph nodes located around the lower third of the internal jugular vein extending from the inferior border of the cricoid cartilage (above) to the clavicle below.
Level V (posterior triangle) This group is comprised predominantly of the lymph nodes located along the lower half of the spinal accessory nerve and the transverse cervical artery. The supraclavicular nodes are also included in posterior triangle group. The superior boundary is the apex formed by convergence of the sternocleidomastoid and trapezius muscles, the inferior boundary is the clavicle, the anterior (medial) boundary is the posterior border of the sternocleidomastoid muscle, and the posterior (lateral) boundary is the anterior boundary is the anterior border of the trapezius muscle.
A horizontal plane marking the inferior border of the anterior cricoid arch separates sublevels.
Sublevel V-A: Above this plane, includes the spinal accessory nodes.
Sublevel V-B: Below this plane, includes the node sthat follow the transverse cervical vessels and the supraclavicular nodes (with the exception of the Virchow node which is located in level IV).
Level VI (anterior compartment) Lymph nodes in this compartment include the pre-and paratracheal nodes, precricoid (delphian) node, and the perithyroidal nodes including the lymph nodes along the recurrent laryngeal nerves. The superior boundary is the hyoid bone, the inferior boundary is the suprasternal notch, and the lateral boundaries are the common carotid arteries.
TABLE 13.6 Classification of Neck Dissection
1991 classification 2001 classification
  1. Radical neck dissection
  2. Modified radical neck dissection
  3. Selective neck dissection
    1. supraomohyoid
    2. lateral
    3. posterolateral
    4. anterior
  4. Extended neck dissection
  1. Radical neck dissection
  2. Modified radical neck dissection
  3. Selective neck dissection (SND):
    1. SND (I-III/IV)
    2. SND (II-IV)
    3. SND (II-V, postauricular, suboccipital)
    4. SND (level VI)
  4. Extended neck dissection
Figure 13.2 Schematic diagram indicating the location of the lymph node levels in the neck.
Figure 13.3 Schematic (A) and intraoperative photograph (B) of the radical neck dissection. (From Bailey BJ, et al., eds. Head and neck surgery otolaryngology. Philadelphia: JB Lippincott, 1993:1200, with permission.)
TABLE 13.7 Classification of Modified Radical Neck Dissections
Type I SCM, IJV (XI is preserved)
Type II SCM (IJV and XI are preserved)
Type III None (SCM, IJV, XI are preserved)
IJV, internal jugular vein; SCM, sternocleidomastoid muscle; XI, cranial nerve XI.
Figure 13.4 Schematic (A) and intraoperative photograph (B) of modified radical neck dissection (type I). (From Bailey BJ, et al., eds. Head and neck surgery otolaryngology. Philadelphia: JB Lippincott, 1993:1202, with permission.)
Figure 13.5 Intraoperative photograph of modified radical neck dissection (type II).
Selective Dissections
Selective neck dissections consist of the removal of only the lymph node groups that are at highest risk for containing metastases, according to the location of the primary tumor. The spinal accessory nerve, the IJV, and the SCM are preserved. Four different neck dissections can be included in this category: lateral neck dissection (lymph node groups II, III, and IV are removed; Fig. 13.7); supraomohyoid neck dissection (lymph node groups I, II, and III are removed; Fig. 13.8); posterolateral neck dissection (the suboccipital and retro-auricular nodes are removed in addition to lymph node groups II, III, IV, and V; Fig. 13.9); and anterior neck dissection (the pretracheal and paratracheal nodes are removed; Fig. 13.10).
The term extended neck dissection is used, in addition to any of the foregoing designations, when a given neck dissection is extended to include either lymph node groups or structures of the neck that are not removed routinely. Such entities as the retropharyngeal nodes or the carotid artery are included.
Figure 13.6 Schematic (A) and intraoperative photograph (B) of modified radical neck dissection (type III). (From Bailey BJ, et al., eds. Head and neck surgery—otolaryngology. Philadelphia: JB Lippincott, 1993:1204, with permission.)
Figure 13.7 Schematic (A) and intraoperative photograph (B) of lateral neck dissection. (From Bailey BJ, et al., eds. Head and neck surgery—otolaryngology. Philadelphia: JB Lippincott, 1993:1207, with permission.)
Figure 13.8 Schematic (A) and intraoperative photograph (B) of supraomohyoid neck dissection. (From Bailey BJ, et al., eds. Head and neck surgery—otolaryngology. Philadelphia: JB Lippincott, 1993:1206, with permission.)
Figure 13.9 A: Schematic representation of the lymph nodes removed by a posterolateral neck dissection. B: Intraoperative photograph.
Figure 13.10 Intraoperative anterior neck dissection.
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PRINCIPLES OF MANAGEMENT OF THE N0 NECK
Indications for Treatment
The clinically negative neck in patients with SCC of the upper aerodigestive tract can be treated with equal success using surgery or radiation therapy. In general, the decision to treat the neck and the choice of treatment modality are dictated by the likelihood of occult lymph node metastases associated with the primary tumor; the modality selected to treat the primary tumor; and, in some instances, the need to enter the neck for reasons of surgical access to the primary tumor.
Treatment of the N0 neck is considered warranted when the probability of occult metastases is greater than 20%. This belief, long held by head and neck surgeons, was reinforced by Weiss et al. (34) using decision analysis to determine the optimal strategy for treatment of the N0 neck as a function of the probability of occult cervical metastases.
Currently, determination of the probability of occult metastases in the lymph nodes is based on various indirect clinical and histopathologic parameters and, when appropriate, imaging studies. That molecular and genetic characteristics of tumors also may be useful in this regard is encouraging.
Imaging Studies
The advent of modern imaging technology brought hopes of reliably identifying metastasis in lymph nodes before they became palpable. Unquestionably, computed tomography (CT) and magnetic resonance imaging (MRI) have a sensitivity and specificity higher than clinical examination in the detection of lymph nodes larger than 1 or 1.5 cm in diameter (35,36,37). Their interpretation relies primarily on the size of the lymph nodes; they cannot distinguish reactive enlargement of a node from enlargement due to metastasis. Though a correlation exists between the size of a lymph node and the probability of its containing metastasis, not all enlarged lymph nodes contain metastatic deposits. Equally important is the observation that, in patients with SCC, a large number of nodes are found to contain metastatic tumor measure less than 1 cm (38). Furthermore, even the presence of a central area of lucency within a node shown on CT, once considered pathognomonic of tumor necrosis within a node (39), can be mimicked by an artery with plaque formation or a fatty inclusion in a lymph node (35). The short and the long axis diameters of enlarged lymph nodes appear to be valuable in differentiating benign and malignant enlargement in cervical lymphadenopathy. In a study by Steinkamp et al. (40), 730 enlarged cervical lymph nodes in 285 patients were examined using ultrasonography, and the long-short (l/s) ratio was calculated. Histologic examination after neck dissection revealed that 95% of enlarged cervical nodes shown ultrasonographically to have an l/s ratio of more than 2 were diagnosed correctly as benign. Nodes presenting with a more circular shape and an l/s ratio of less than 2 were diagnosed correctly as metastases, with 95% accuracy (40).
Multidirectional ultrasound scanning appears more promising for a better preoperative evaluation of the N0 neck (41). It can depict lymph nodes as small as 3 mm in diameter, from which material for cytopathologic examination can be obtained by directed fine-needle aspiration biopsy (35).
Predictors of Nodal Metastases
The incidence of occult lymph node metastases for the different tumors according to site of origin and T stage is outlined in Tables 13.2,13.3 and 13.4 Tumor site and stage are helpful general indicators of the likelihood of occult metastases for a given primary tumor, but they are not completely accurate; hence, the constant search for better ways to determine the presence or absence of metastatic deposits in the lymph nodes.
Available to clinicians today is an increasing number of clinical, histologic, biochemical, and genetic factors that may be useful predictors of the propensity of a tumor to metastasize to the lymph nodes, and these factors may be useful in treatment planning. For example, in one study of 126 patients who had SCC of the oral cavity and underwent neck dissection as part of their treatment, Martinez-Gimeno et al. (42) found a statistically significant association between lymph node metastasis and the presence of microvascular invasion, grade of differentiation, tumor thickness, inflammatory infiltration, tumoral interphase, and the presence of perineural spread. On the basis of their results, these investigators designed a scoring system with a range of points from a to d. Scoring was done as follows: a, 7 to 12 points; b, 13 to 16 points; c, 17 to 20 points; and d, 21 to 30 points. The respective risk for metastasis was: a, 0%; b, 20%; c, 63.6%; and d, 86.3%.
TUMOR THICKNESS
The incidence of nodal metastases in patients with SCC of the floor of the mouth and oral tongue appears to increase as a function of the thickness of the primary tumor. In 1986, Mohit-Tabatabai et al. (43) found a significant correlation between tumor thickness of greater than 1.5 mm and subsequent development of neck metastases in a series of patients with stage I and stage II carcinomas of the floor of the mouth. In the same year, Spiro et al. (44), in a study of 105 patients with oral and oropharyngeal carcinoma with N0 necks, found that lymph node metastases occurred more frequently in patients whose tumors measured at least 2 mm thick.
By the use of mathematic modeling, the estimated risk for cervical node metastasis relative to thickness of SCC of the oral cavity was found to be approximately 3.9% for cancers 1-mm thick, 17% for cancers 2-mm thick, and 25% for cancers 3-mm thick (45). Similar findings by Frierson and Cooper (46) in patients with carcinoma of the lower lip and by Rasgon et al. (47) in patients with oral and oropharyngeal carcinoma support the importance of thickness as a predictor of nodal metastases. However, its usefulness in planning treatment of the neck is limited by the difficulty in determining tumor thickness through inspection or in biopsy specimens.
HISTOLOGIC GRADE
Despite the absence of general agreement about the prognostic impact of histologic differentiation, several studies have demonstrated a higher incidence of neck node metastases in patients with poorly differentiated SCC (22,46, 48,49). In oral cavity tumors, a higher grade of malignancy in terms of degree of differentiation and character of the borders may increase risk for metastases beyond the first and second echelon of regional lymph nodes (50) and may increase the risk for occult metastases in lower levels of the neck.
INVASIVE MARGIN OF THE TUMOR
More recently, attention has focused on the “malignancy grading” and character of the invasive margin of the tumor (pushing vs. infiltrating). Bryne et al. (51) have shown that patients with oral cavity carcinomas that exhibit an infiltrating margin with abundant mitoses and nuclear polymorphism are associated with a dismal survival. Others have shown an increased risk for occult lymph node metastases for such tumors (46,48,50,52,53).
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VASCULAR INVASION
The role of vascular invasion as a risk factor for lymph node metastases is unclear. In a study of 43 patients, Close et al. (54) found lymph node metastases in 77% of the cases in which vascular invasion was present but in only 25% of the cases in which it was absent. Though Crissman et al. (53) and Poleksic and Kalwaic (55) have found a similar correlation, others have not (46,47).
PERINEURAL INVASION
Several studies have suggested a strong correlation between the presence of perineural invasion at the primary site and cervical lymph node metastases (46,48).
INFLAMMATORY INFILTRATE
A marked inflammatory infiltrate in the stroma surrounding the tumor has been found to correlate with a lower incidence of lymph node metastases in some studies (43,46,48). Other studies have not shown such correlation (49,53,54).
DNA PLOIDY
Data from the literature are contradictory concerning the therapeutic and prognostic implications of DNA content in tumors of the head and neck. On the one hand, several investigators have found that cervical lymph node metastases are more frequent in patients with DNA nondiploid tumors than in similar patients with diploid tumors (56,57). In a study of 94 cases with advanced laryngeal cancers, ploidy was determined by computerized cytomorphometry. A high adjusted DNA index was associated with a higher incidence of lymph node metastases and with a higher number of histologically positive nodes (58).
However, just as many investigators have not been able to demonstrate such clear correlations (59,60). These differences, most likely due to the varying methods used by the different laboratories, limit the clinical applicability of DNA content analysis in decisions concerning treatment of the N0 neck.
TUMOR ANGIOGENESIS
Tumor angiogenesis has been associated with metastasis in breast, prostate, and non-small cell lung cancers. For head and neck SCC, Williams et al. (61) report that angiogenesis as determined by immunostaining of endothelial cells for factor VIII-related antigen was related strongly to the probability of metastasis in a group of 66 patients with oral cavity tumors and N0 necks. However, Leedy et al. (62) report, in a series of 57 patients who had tongue tumors and both N0 and N+ necks, that tumor angiogenesis was of no predictive value.
INTEGRITY OF THE BASEMENT MEMBRANE
Continuity of the basement membrane appears to be a predictor of nodal metastases, independent of T stage and differentiation. Murakami et al. (63) have investigated the immunohistologic localization and continuity of type IV collagen in the basement membrane surrounding the “cancer nest” into the stroma. These authors found that membrane discontinuity (breaks or absence) correlated significantly with cervical lymph node metastasis, whereas intact membrane was associated with a low frequency of cervical lymph node metastasis.
TABLE 13.8 Treatment of N0 Neck
Location of primary Oral cavity Oropharynx Hypopharynx Larynx
BOT Tonsil pharyngeal walls
Type of neck dissection SND I–III/IV SND II–III (IV) SND II–IV Retropharyngeal SND II–IV Retropharyngeal SND II–IV (Subglottic: level VI)
BOT, base of tongue; SND, selective neck dissection.
Surgical Treatment
INDICATIONS
Surgical treatment of the N0 neck is preferred when surgery is selected for the treatment of the primary tumor, particularly when the expectations of controlling the primary tumor with surgery alone are reasonably good. In such cases (e.g., T2 and selected T3 tumors of the oral cavity, T1 and T2 tumors of the supraglottic larynx), appropriate dissection of the regional lymph nodes alone is, in most cases, sufficient to control the disease in the neck. However, postoperative radiation therapy may be beneficial when the following features are found on histopathologic examination of the node dissection specimen(s):
  • Presence of tumor in more than two or three lymph nodes
  • Presence of tumor in multiple node groups
  • Presence of extracapsular extension of tumor
Surgical dissection of the cervical lymph nodes also is desirable to facilitate adequate resection of the primary tumor when the neck must be entered and certain structures, such as the hypoglossal nerve or the carotid artery, must be exposed.
TYPE OF NECK DISSECTION
Radical neck dissection and modified RNDs are being used by fewer surgeons for the treatment of the N0 neck. Instead, selective neck dissections increasingly are accepted in the surgical treatment of the N0 neck (Table 13.8). These neck dissections are predicated on the basis of several observations.
As shown in Tables 13.3 and 13.4 (3,4,64,65,66), nodal metastases are found in predictable regions of the neck, depending on the site of the primary tumor. In a retrospective study that included 914 patients who underwent a lymph node dissection, the sentinel nodes for well-lateralized oral cavity tumors were defined as the homolateral levels I, II, and III; for oropharyngeal, hypopharyngeal, and laryngeal tumors, the sentinel nodes were defined as levels II and III (66).
En bloc removal of only the lymph node groups at highest risk for harboring metastases appears to have the same therapeutic value and provides the surgeon with the same staging information as the more extensive RNDs and modified RNDs (67,68,69). The morbidity associated with these operations is minimal and potentially reversible (70,71).
Two operations are included in this category of neck dissections:
TABLE 13.9 Lateral Neck Dissection Recurrence within Dissected Side of the Neck (Primary Controlled, 2-Year Follow-up)
Pathologic staging Medinaa
Surgery only (%)
Byersb
Surgery only (%)
Medina
Surgery + irradiation (%)
Byers
Surgery + irradiation (%)
N0 0 of 15 (0) 10 of 130 (8) 1 of 19 (5.2) 1 of 126 (1)
N1 0 of 4 (0) 0 of 3 (0) 0 of 17 (0)
Multiple nodes; extracapsular extension 0 of 6 (0) 3 of 20 (15)
aUniversity of Oklahoma experience.
bData modified from Byers RM. Modified neck dissection: a study of 967 cases from 1970 to 1980. Am J Surg 1986;150:414–421.
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  • The lateral neck dissection consists of the en bloc removal of nodal regions II, III, and IV. This procedure is indicated in patients with tumors of the larynx, oropharynx, and hypopharynx staged T2 through T4 N0. Because the lymphatic drainage of these regions is such that metastases frequently are bilateral, often the operation is performed on both sides of the neck. The results obtained with this operation are shown in Table 13.9.
  • The supraomohyoid neck dissection consists of the en bloc removal of nodal regions I, II, and III. It is the preferred procedure for the surgical management of patients with SCC of the oral cavity. The procedure is performed on both sides of the neck in patients with cancers of the anterior tongue and floor of the mouth. This type of dissection is also performed when an elective neck dissection is indicated in the management of patients who have SCC of the lip or skin in the midportion of the face.
A bilateral dissection is performed when the lesion is located at or near the midline.
Postoperative radiation therapy is used when metastases are found in multiple nodes at one level or in nodes at multiple levels or when ECS of tumor is present.
In a prospective analysis of our practice (70), the use of supraomohyoid and lateral neck dissections in this manner produced a rate of recurrence in the neck that ranged from 0% (when the removed nodes were histologically negative) to 12.5% (in the presence of multiple positive nodes or ECS) (Table 13.10). Similar results of 5% to 15% and 5% to 21% have been reported by Byers (65) and Spiro et al. (67), respectively. In a more recent prospective study, a recurrence in the neck after supraomohyoid neck dissection occurred in 4 of 34 patients (11.7%) with T1 to T2 SCC of the oral cavity (71). Others have reported similar results (72).
TABLE 13.10 Supraomohyoid Neck Dissection Recurrence within Dissected Side of the Neck (Primary Controlled, 2-Year Follow-up)
Pathologic staging Surgery only (%) Surgery and postoperative radiation therapy (%)
Medinaa Byersb Medina Byers
N0 0 of 51 7 of 30 (5) 1 of 29 (3.45) 2 of 24 (8)
N1 1 of 10 (10) 0 of 3 0 of 8
Multiple nodes, extracapsular extension 0 of 1 5 of 21 (24) 2 of 16 (12.5) 6 of 41 (15)
aUniversity of Oklahoma experience.
bData modified from Byers RM. Modified neck dissection: a study of 967 cases from 1970 to 1980. Am J Surg 1986;150:414–421.
Intraoperative Staging of the N0 Neck
Incorrect clinical staging of the N0 occurs in approximately 20% of patients, even when imaging studies are used. Rassekh et al. (73) addressed the issue of intraoperative staging of the neck in a prospective study of 108 neck dissections. Intraoperative palpation and inspection did not significantly improve the surgeon’s ability to predict nodal stage. Of 62 patients with clinical N0 necks on both sides, 26 were staged N+ by intraoperative node examination. Nineteen of these 26 were histologically negative (73% false-positive). Of the 36 patients intraoperatively staged as N0, 10 were histologically positive (28% false-negative). Thus, upstaging the neck without frozen-section examination of suspected lymph nodes is not reliable. Although these authors recommended converting the selective dissection to an RND or modified RND on the basis of the results of frozen sections, this route has not been found necessary in our experience. Removal of the SCM, the IJV, or the posterior triangle of the neck is not performed unless these areas are obviously involved by the tumor. The decision to extend a selective neck dissection to include the jugular vein, the spinal accessory nerve, or (occasionally) the hypoglossal or the vagus nerve is based on the findings at the time of surgery and on an objective assessment of the extent of nodal disease by the surgeon.
An anterior compartment dissection (removal of the pretracheal and paratracheal lymph nodes) seldom is performed alone. It is indicated as part of the surgical treatment of tumors of the thyroid, subglottic larynx, trachea, and cervical esophagus.
TABLE 13.11 Recurrence Rates in the N1 Neck After Selective Neck Dissection
Neck dissection type Total Surgery (%) Surgery + radiation (%) Other (%)
Supraomohyoid 92 10 of 44 (23) 13 of 46 (28) 1 of 2 (50)
Lateral 26 3 of 8 (38) 2 of 18 (11)
Total 118 13 of 52 (25) 15 of 64 (23) 1 of 2 (50)
Source: Data from Houck JR, Medina JE. Management of cervical lymph nodes in squamous carcinomas of the head and neck. Semin Surg Oncol 1995;11:228–239.
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Elective Neck Irradiation
The N0 neck is treated with radiation therapy in patients in whom the primary tumor is irradiated, and in whom the likelihood of occult nodal metastases is 20% or higher. Radiation therapy is also used in patients in whom postoperative treatment is indicated on the basis of the characteristics of the primary tumor alone (T4 and infiltrating T3 tumors) and when these can be resected adequately without entering the neck. Fletcher (74) and others have shown that the risk for developing clinically positive nodes in an N0 neck can be reduced to perhaps 5% with the use of comprehensive neck irradiation (75).
MANAGEMENT OF THE N+ NECK
Surgery continues to be the mainstay in the treatment of patients with palpable cervical lymph node metastases. A notable exception is the treatment of the neck in patients with nasopharyngeal carcinoma in which even large nodal metastases are controlled readily with radiation. A neck dissection is indicated only when radiation has controlled the primary tumor but has failed to control the tumor in the neck (76,77).
Imaging Studies
Preoperative imaging of extensive metastases in the neck with CT and MRI has focused mainly on assessment of resectability. A more recent and intriguing focus is the use of image analysis in predicting response to therapy. Nodal density, as compared with the density of nuchal muscles in contrasted CT scans, has been shown to have a strong correlation with response to cisplatin-based chemotherapy (78). This concept merits further evaluation.
In terms of assessing resectability, CT scanning and MRI enable surgeons to define more clearly the relationship of a metastatic tumor to such critical structures as the common and the internal carotid arteries, the cervical spine and the vertebral artery, and the brachial plexus. The advantages of having such information in advance are obvious, particularly when tumor involvement of the common or the internal carotid artery is suspected. Such a case renders it desirable to assess accurately the structural and functional status of the contralateral carotid and the collateral intracerebral circulation. Angiography now is complemented routinely by measuring carotid backpressure and using balloon occlusion techniques while monitoring the patient for evidence of neurologic deficits under normotensive and hypotensive conditions (79).
TABLE 13.12 Recurrence Rates in the Neck After Type I Modified Radical Neck Dissections
Study No. of dissections Follow-up (mos) Percentage of recurrence
Elective procedure Therapeutic procedure
Pearlman et al. (81) 56 18 7 20
Bradenburg and Lee (82) 65 60 5 11
69 24 4 5
Roy and Beahrs (83) 89 40 4 17
Skolnik et al. (84) 42 0 0
Chu and Strawitz (85) 21 24 5
Carenfelt and Eliasson (86) 81 53 9
Andersen et al. (87) 132 38 8
Surgical Treatment
As more surgeons accept the surgical and oncologic feasibility of removing involved lymph nodes along with surrounding fibrofatty tissue (but without removal of such important uninvolved structures as the spinal accessory nerve), the surgical management of the N+ neck is becoming a matter of judgment. In addition, with the judicious combination of surgery and radiation therapy, excellent tumor control in the neck can be obtained while preserving function and cosmesis (65). The main goal of neck dissection is, however, to adequately remove the tumor from the neck and not to rely on radiation therapy to compensate for poor surgical technique. Preservation of adjacent structures should be pursued only when a clearly identifiable plane exists between the tumor and that structure. Cutting into and spilling of tumor must be avoided.
The results obtained with selective neck dissection in patients with stage N1 disease, in which the node is less than 3 cm in diameter, is mobile, and is located in the first echelon of lymphatic drainage (80) are listed in Table 13.11. For more advanced nodal metastases, Tables 13.12 (81,82,83,84,85,86,87) and 13.13 (88,89,90,91,92,93) show the rates of tumor control in the neck reported
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with modified RND. These results appear to be comparable to those obtained with RND. Andersen et al. (94) reviewed the results of 378 neck dissections performed in 366 patients with clinically and pathologically positive nodal metastases from SCC of the upper aerodigestive tract. The study compared survival and tumor recurrence in the neck in patients who had RND with those who had modified RND with preservation of the spinal accessory nerve. Preservation of the spinal accessory nerve did not affect survival and tumor control in the neck. Interestingly, the pattern of failure in the neck was similar for the two operations.
TABLE 13.13 Recurrence Rates in the Neck with Type III Modified Radical Neck Dissection
Study No. of dissections Follow-up (mos) Recurrence rate (%) for elective procedures Recurrence rate (%) for therapeutic procedures
N0 N1 N+ N2
Lingeman et al. (88) 59 0 15.0 25
Molinari et al. (89) 128 36 1.3 3.7
Joseph et al. (90) 18 18 16.5 0
Gavilan and Gavilan (91) 242 60 8.9 7.9 20
Bocca et al. (92) 843 60 2.4 30.4
Calearo and Teatini (93) 258 36 3.2a 5.6b
aClinically and histologically node-negative.
bClinically and histologically node-positive. In these cases, authors did not distinguish between N1 and N2.
Postoperative Radiation Therapy
Numerous studies suggest that when multiple nodes are involved at multiple levels of the neck and when ECS of tumor is found, the rate of tumor recurrence in the neck is decreased by the addition of radiation therapy (13,15,17,95,96). The timing and the dose of radiation therapy are crucial if good regional control is to be achieved. Results of one prospective clinical trial provide the basis for the recommendation that patients with advanced head and neck cancer treated with daily fractions of 1.8 Gy should receive a minimum postoperative dose of 57.6 Gy to the entire operative bed. Sites of increased risk for recurrence, such as areas of the neck wherein ECS of tumor was found, should be boosted to 63 Gy. Radiation therapy should be started as soon as possible after surgery (97). Some studies have suggested that a delay in the initiation of radiation therapy beyond 6 weeks may compromise tumor control (96), but this caution has been disputed.
Large doses of radiation intraoperatively delivered to the neck may be useful in the treatment of patients with advanced cervical metastases. Freeman et al. (98) report one of the largest experiences with this technique. Seventy-five patients who had advanced cervical metastasis with possible invasion of the deep muscles or carotid artery were approached with aggressive resection and intraoperative radiation therapy (IORT). All metastatic nodes were greater than 3 cm, 65% were fixed on clinical examination, and 35% involved the carotid artery. Fifteen of the patients required extended neck dissections with carotid resections and grafting. After the resection, an average single dose of 2,000 cGy of electron beam IORT was delivered. At 2 years, the local control rate within the IORT port was 68% (98). This technique requires a sophisticated and expensive setup in the operating suite and requires cumbersome transport of an anesthetized patient with a large open wound to the radiation therapy facility.
SPECIAL ISSUES IN THE TREATMENT OF THE NECK
Resection of the Carotid Artery
The extent of the tumor in the neck may dictate the need to extend a neck dissection to include such structures as the hypoglossal nerve, the carotid, and the overlying skin, none of which normally is removed by this operation. The controversy about the advisability of resecting the common or the internal carotid artery has not been resolved. Some surgeons still believe that carotid resection in patients with advanced SCC of the neck does not improve long-term survival (102), even though improved techniques for vascular and soft-tissue reconstruction have rendered possible the resection of the carotid with acceptable morbidity (100,101).
Advanced Neck Metastases with a Small Primary Tumor
Advanced metastasis occurs more often with carcinomas of the oropharynx or hypopharynx. Treatment can consist of (a) excision of the primary tumor, concomitant neck dissection, and postoperative radiation or (b) radiation therapy to the primary tumor and the neck, followed by neck dissection 4 to 6 weeks later. The latter approach is preferred by some surgeons because the primary tumor is small and usually is located in an area in which preservation of function is more likely with radiation, such as the soft palate, base of the tongue, or hypopharynx. This approach, however, presents two significant drawbacks: (a) the uncertainty of tumor control at the primary site 4 to 6 weeks after completion of radiation therapy and (b) the intraoperative and postoperative consequences on tissue planes and healing of radiation.
A new treatment alternative to this problem was reported by the surgeons at the M. D. Anderson Cancer Center (102), where a neck dissection was performed first and was followed by radiation therapy (a postoperative dose to the neck and a definitive dose to the primary tumor). In a selected group of 35 patients with advanced neck disease (median size, 5×4 cm) and primary tumors thought to be amenable to treatment by radiation therapy, recurrence of tumor in the neck occurred in only 11% of the patients; the overall 5-year survival was 55%. Using a similar treatment approach in 65 patients with tumors of the larynx and hypopharynx, the French Head and Neck Study Group observed a rate of recurrence in the neck of 4.6% (103).
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For this treatment approach to succeed, the resectability of the tumor in the neck must be assessed carefully, and the neck dissection must be performed meticulously, with care to avoid complications that may delay the initiation of radiation. Furthermore, the radiation oncologist must be willing to begin therapy as soon as a few days after surgery. In this study, delaying the start of radiation therapy for more than 2 weeks was associated with a significant decrease in survival.
Treatment of the Neck and Neoadjuvant Chemotherapy
Decisions about treatment of the neck deserve special consideration when neoadjuvant chemotherapy and radiation therapy are used for organ preservation in patients with palpable cervical lymph node metastases. In this regard, valuable information has been provided by an analysis of a subset of 92 patients who had laryngeal carcinoma and advanced neck disease (N2 or N3) and were treated as part of the Veterans Administration Cooperative Study (104) of induction chemotherapy (cisplatin and 5-fluorouracil) and definitive radiation (6,600-7,600 cGy). After chemotherapy and radiation, a neck dissection was necessary in 68% of the patients in whom the tumor in the neck exhibited less than a complete clinical response to the induction chemotherapy and in 28% of the patients in whom a complete response was observed. Armstrong et al. (105) have reported similar observations.
Though the authors of these studies recommend a neck dissection be performed only when less than a complete response to chemotherapy occurs, arguably a 28% probability of persistent tumor in the neck justifies also performing a neck dissection in patients who have a complete clinical response to chemotherapy. After all, most head and neck surgeons recommend treating the N0 neck when the probability of occult metastases is 20% or higher. This argument is strengthened by the fact that 60% of those patients died of uncontrolled disease in the neck, despite salvage neck dissection (104).
Sequelae of Neck Dissection
SCAPULAR DESTABILIZATION
The most troublesome sequelae after RND result from the removal of the spinal accessory nerve and denervation of the trapezius muscle. The resultant destabilization of the scapula leads to drooping and lateral and anterior rotation followed by progressive flaring away from the vertebral column posteriorly. The loss of the trapezius function decreases the patient’s ability to abduct the shoulder above 90 degrees. These physical changes result in the recognized shoulder syndrome of pain, weakness, and deformity of the shoulder girdle commonly associated with RND (Fig. 13.11). These effects all are accentuated in patients who are overweight, in whom the weight of tissue anteriorly increases the anterior forces.
In the last few years, the literature has reflected debate over whether a significant difference is seen in postoperative shoulder function after an RND and the modifications of RND that preserve the spinal accessory nerve. Using patient questionnaires, Schuller et al. (106) compared symptomatology and the ability to return to preoperative employment in patients who underwent either an RND or a modified RND. Though they found no statistically significant difference between the two groups, Sterns and Shaheen (107) and others (108; R. Byers, personal communication, 1994), using methods similar to Schuller’s, found that most patients who had a nerve-sparing procedure did not have postoperative pain or shoulder dysfunction.
Figure 13.11 Shoulder deformity characteristic of denervation of the trapezius muscle.
Only recently have prospective objective data on shoulder dysfunction after neck dissection been gathered. Leipzig et al. (109) studied 109 patients who had undergone various types of neck dissections. They used the surgeon’s preoperative and postoperative observations of shoulder movement rated by the degree of shoulder dysfunction. The authors concluded that any type of neck dissection could result in impairment of function of the shoulder. Dysfunction, however, occurred more frequently among those patients in whom the spinal accessory nerve was dissected or resected extensively.
In a 1986 prospective study, Sobol et al. (69) compared preoperative and postoperative measures of shoulder range of motion. In some patients, postoperative electromyograms (EMGs) also were obtained. Shoulder range of motion in patients who underwent a nerve-sparing procedure was better than in those who had an RND. Interestingly, however, the type of nerve-sparing procedure was found to affect the degree of shoulder disability. Sixteen weeks after surgery, patients who had undergone a modified RND (in which the entire length of the nerve was dissected) did not have shoulder range of motion better than that in patients who had a standard RND. However, patients who underwent a supraomohyoid neck dissection (embodying less extensive dissection of the spinal accessory nerve) performed significantly better (p ≥ 0.05) than did either of the other two groups, both in terms of shoulder range of motion and EMG findings on the trapezius muscle. Importantly, at 16 weeks after surgery, moderate to severe EMG abnormalities were noted in as many as 65% of the patients in whom the spinal accessory nerve was dissected in its entire length (modified RND). Though no severe abnormalities were noted in the group undergoing supraomohyoid neck dissection, 22% of them showed moderate abnormalities.
Several patients from each group had repeat studies at 1 year after a surgery. Unlike the outcome in the patients who had had an RND, clear evidence of improvement in all parameters studied was seen in patients in whom the nerve was spared.
Figure 13.12 Patient with denervated trapezius and shoulder drooping several years after modified radical neck dissection with preservation of internal jugular vein, sternocleidomastoid muscle, and XI nerve (type III).
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A more recent prospective study by Remmler et al. (68) also revealed that patients who had a nerve-sparing procedure experienced a significant but temporary phase of spinal accessory nerve dysfunction. In this study, preoperative strength, range-of-motion measures, and EMG of the trapezius muscle were compared with postoperative measures obtained at 1, 3, 6, and 12 months. The groups studied consisted of patients undergoing nerve-sparing procedures and those in whom the nerve was resected. Most of the patients in the nerve-sparing group had supraomohyoid neck dissections. Patients who underwent RND had a significant decrease in trapezius muscle strength and underwent denervation of the trapezius muscle on EMG at 1 month; these parameters did not improve with time. Interestingly, patients in the nerve-sparing group had a small but significant reduction in trapezius muscle strength and evidence of trapezius muscle denervation at 1 and 3 months, which improved by 12 months.
The last three studies have provided evidence that even procedures involving minimal dissection of the spinal accessory nerve can result in shoulder dysfunction (Fig. 13.12). Although this outcome appears to be reversible, every effort should be made to avoid undue trauma to the nerve (particularly stretching) during any neck dissection in which the nerve is preserved. Furthermore, every patient who undergoes neck dissection must be questioned about the function of the shoulder and must be evaluated by a physical therapist early in the postoperative period. Should any deficit be detected, the patient should be counseled and coached properly to ensure proper rehabilitation of the shoulder.
Surgical Complications
In addition to the medical complications that can occur after any surgical procedure in the head and neck region, several surgical complications can be related solely or in part to the neck dissection.
AIR LEAKS
Circulation of air through a wound drain is a common complication usually encountered during the first postoperative day. The point of entrance of air may be located somewhere along the skin incision. However, if the drains are connected to suction in the operating room just before the completion of the wound closure, such an air leak usually becomes apparent at that time and can be corrected. Other points of entrance may not become apparent until after surgery, when the position of the neck changes or the patient begins to move. The typical example of this situation is the improperly secured suction wound drain that becomes displaced, thus exposing one or more of the drain vents.
Air leaks with potentially more serious consequences are those that occur through a communication of the neck wound with the tracheostomy site or through a mucosal suture line. In these, air and contaminated secretions enter the neck wound. Early identification of the site of leakage, therefore, is desirable. Doing so may not be a simple task, however, and correction may require revision of the wound closure in the operating room.
BLEEDING
Postoperative hemorrhage usually occurs immediately after surgery. External bleeding through the incision without distortion of the skin flaps often originates in a subcutaneous blood vessel. In most instances, this effect can be controlled readily by ligation or infiltration of the surrounding tissues with an anesthetic solution containing epinephrine. On the other hand, pronounced swelling or ballooning of the skin flaps during the immediate postoperative period must be attributed to a hematoma in the wound, even if bleeding is not obvious. If the swelling or ballooning is detected early, manipulating the drains occasionally results in evacuation of the accumulated blood and resolves the problem; however, if this is not accomplished immediately or if blood reaccumulates quickly, the best response is to return the patient to the operating room to explore the wound under sterile conditions, to evacuate the hematoma, and to control the bleeding. Attempting to do this in the recovery room or at the bedside usually is ill advised because lighting may be inadequate, surgical equipment may have to be improvised, and sterile conditions can be compromised. Failure to recognize or to manage a postoperative hematoma properly may predispose the patient to the development of wound infection. Although bulky pressure dressings may be useful in curtailing postoperative edema, they do not prevent hematomas and may, in fact, delay their recognition.
Jugular vein rupture should be considered in patients who have undergone primary tumor excision with modified RND and in whom the procedure is complicated by a pharyngocutaneous fistula. In this circumstance, the bleeding is venous and occurs repeatedly (110).
CHYLOUS FISTULA
Despite the best efforts of surgeons, a postoperative chylous fistula occurs after 1% to 2% of neck dissections (111). Spiro et al. (112) reviewed 823 neck dissections that included removal of the lymph nodes in level IV. They found that in most patients who developed a chylous fistula, a chylous leak had been identified intraoperatively but was thought to be under control intraoperatively in most patients who developed a chylous fistula (111,112). It behooves the surgeon, therefore, to avoid injury to the thoracic duct proper and also to ligate or clip even potential lymphatic tributaries in the area of the thoracic duct. This precaution may be accomplished with relative ease if the operative field is kept bloodless during dissection in this area of the neck. Furthermore, as soon as the dissection of this area is completed and again before closing the wound, the area is observed for 20 or 30 seconds while the anesthesiologist increases the intrathoracic pressure.
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Even the smallest leak of chylous material must be pursued seriously until it is arrested. Direct clamping and ligating may be difficult and sometimes counterproductive, owing to the fragility of the lymphatic vessels and the surrounding fatty tissue. Hemoclips are ideal to control a source of leakage that is visualized clearly. Otherwise, use of suture ligatures is preferable (with pliable material, such as 5-0 silk). They should be tied over a piece of hemostatic sponge to avoid tearing.
Management of this complication depends on the time of onset of the leak and the amount of chyle drainage in a 24-hour period and on the ability of the physician to prevent accumulation of chyle under the skin flaps. When the daily output of chyle exceeds 500 mL to 600 mL, especially when the chyle fistula becomes apparent immediately after surgery, conservative closed-wound management is unlikely to succeed. In such cases, we prefer early surgical exploration, before the adjacent tissues become markedly inflamed and before the fibrinous material that coats these tissues becomes adherent, thus obscuring and jeopardizing such important structures as the phrenic and the vagus nerves. Chylous fistulae that become apparent only after enteral feedings are resumed and particularly those that drain less than 600 mL of chyle per day initially are managed conservatively with closed wound drainage and low-fat nutritional support.
FACIAL AND CEREBRAL EDEMA
Synchronous bilateral RNDs in which both IJVs are ligated can result in the development of facial edema, cerebral edema, or both. Sometimes, the facial edema can be severe (Fig. 13.13). This effect appears to be a mechanical problem of venous drainage, which resolves to a variable extent with time as collateral circulation is established. Such swelling is more common and more severe in patients who had previous radiation to the head and neck and in those patients in whom the resection includes large segments of the lateral and posterior pharyngeal walls.
Figure 13.13 Severe facial edema that can occur after bilateral neck dissection.
We have been able to prevent massive facial edema by preserving at least one external jugular vein whenever a bilateral RND is anticipated. The external jugular vein usually is separated from the tumor in the neck by the SCM and can be dissected free between the tail of the parotid and the subclavian veins (Fig. 13.14). Others recommend grafting of one of the IJVs.
After bilateral RND, the development of cerebral edema may cause impaired neurologic function and even coma. Ligation of the IJVs leads to increased intracranial pressure (113,114). In a study by Weiss et al. (34), four patients who had staged bilateral RNDs underwent placement of a subarachnoid bolt for direct monitoring of intracranial pressure. Marked elevations of pressure were noted immediately after ligation of the IJV, with a maximum peak at 30 minutes. Furthermore, systemic hypertension was observed in response to elevated intracranial pressure (Cushing reflex). Also, the increased cerebral venous pressure that occurs as a result of ligating both IJVs in dogs has been shown experimentally to be associated with inappropriate secretion of antidiuretic hormone (115). One then can speculate that the resulting expansion of extracellular fluids
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and dilutional hyponatremia could aggravate cerebral edema, creating a vicious cycle.
Figure 13.14 Dissection of the external jugular vein from the parotid to the supraclavicular region before performing a radical neck dissection.
In practice, these observations behoove the surgeon and the anesthesiologist to curtail the administration of fluids during and after bilateral RNDs (116). Furthermore, perioperative management of fluid and electrolytes in these cases should not be guided solely by the patient’s urine output but additionally by monitoring of central venous pressure, cardiac output, serum, and urine osmolarity. Also interesting to note is that after bilateral neck dissection, some patients may lose their hypoxic ventilatory responses, owing to carotid body denervation (117).
BLINDNESS
Blindness after bilateral RND is a rare but catastrophic complication. To date, five cases have been reported in the literature (118). Posterior ischemic optic neuropathy after bilateral RND may be related to hypotension. In one report, histologic examination revealed intraorbital optic nerve infarction, suggesting as possible etiologic factors intraoperative hypotension and severe venous distention. Thus, avoiding drug-induced hypotension is important for preventing this complication (119).
JUGULAR VEIN THROMBOSIS
Preservation of the IJV during neck dissection does not ensure its postoperative patency, particularly when radiation therapy also is used. In a retrospective study using cervical duplex and pulsed Doppler imaging to determine IJV patency after modified RND, the rate of patency of the IJV was found to be 87% (120). Cotter et al. (121) used preoperative and postoperative CT or MRI on 69 patients undergoing 79 vein-sparing neck dissections. Sixty-eight veins (86%) were patent after surgery (121). Interestingly, radiation therapy appears to influence patency of the IJV. Through noninvasive color Doppler ultrasonography scan, the IJVs were found to be normal bilaterally in 18% of patients who had undergone a modified RND and radiation therapy, in 88% of patients who had undergone a neck dissection alone, and in 57% of patients who had undergone radiation therapy alone (122).
RADIOLOGIC IMAGING CONCERNS
Bernard B. O’Malley
Suresh K. Mukherji
The main roles for imaging of the neck for surgical management include confirming the N0 status of the neck, excluding nodal metastases contralateral to clinically palpable disease, the extent of bulky adenopathy, and evaluation of the posttreatment neck. Imaging the neck for metastatic disease is an adjunct to clinical palpation. Imaging is especially important in obese patients or patient with thick necks. Diagnosing adenopathy in the neck is based on morphology by CT (Fig. 13.15), MRI, or ultrasonography (126,127,128). Computed tomography imaging requires intravenous contrast. Contrast is also beneficial in MRI for evaluating central areas of low attenuation, which may represent small focal metastases. Other imaging modalities, which may also be used to evaluate the neck, include radioimmunoscintigraphy, positron emission tomography scanning (129), and iron-dextran enhanced MRI (130,131). These latter methods along with Doppler ultrasonography provide a more accurate physiologic evaluation of lymph nodes. Sonography adds little to the work-up if contrast CT has been performed except for higher specificity when used to guide fine-needle aspiration (132).
Computed tomography and MRI (Fig. 13.16) are the primary diagnostic modalities used in North America for staging the neck. The slice thickness should not exceed 5 mm with either modality, and many institutions prefer 3-mm thick sections for CT. The imaging should begin at the skull base and extend inferiorly to the level of the head of the clavicles (Fig. 13.17). To obtain adequate vascular opacification with CT prior to imaging, approximately 30 to 50 cc are required prior to acquiring the first image. The exact timing of the bolus and the delay in imaging varies with specific types of CT scanners (Fig. 13.18). No such delay is required with MRI after contrast administration.
Standard cross-sectional CT and MRI are based on lymph node morphology size and enhancement features. Adjunctive methods can be applied with better accuracy when scans are equivocal. Doppler analysis of the intrinsic blood flow has been shown to be beneficial in characterizing suspicious nodes even before they are enlarged (133). Conventional sonography is less sensitive than CT, MRI, or fluorodeoxyglucose-positron emission tomography (FDG-PET) (134). The benefit of sonography is the convenience of performing a fine-needle aspiration if the node remains suspicious. Fine-needle aspiration is an efficient and highly accurate method for confirming or excluding nodal metastases (135). Nuclear imaging with thallium-201 (136) can help reduce the false-positive cross-sectional results. The use of FDG-PET is now established as a very powerful adjunct to staging the head and neck (137).
Accurate staging of the neck opposite to the side of palpable nodal disease is essential for proper treatment of the neck. The risk for contralateral nodal metastases contributes to the morbidity of bilateral neck treatment. Careful analysis will help to differentiate among the subgroups of N2 disease (138). One must be familiar with the typical lymphatic drainage patterns for the various primary sites so as to avoid false-positive lymph node staging (Fig. 13.19). On a similar theme, one must be aware of the typical neck dissections associated with the various primary sites and should bring to the surgeon’s attention any suspicious lymph node findings that may fall out of that standard operative approach (139). Among the adverse prognostic factors of cervical nodal metastases is the number of levels involved and ECS. Extracapsular penetration can be diagnosed by obliteration of the normal fat plane surrounding a metastatic lymph node. Tumors that have imaging evidence of extending across midline or those arising from midline structures such as palate, tongue base and supraglottic, are at greater risk for metastases to the contralateral neck.
Another important role of neck imaging is the regional evaluation of a known aggregate nodal mass relative to the adjacent neurovascular structures and to evaluate invasion of deep neck muscle before invasion. This information is important as the presence of carotid encasement or invasion of the deep neck muscles renders patients unresectable at many institutions. Carotid invasion can be suggested if a tumor surrounds the carotid artery by more than 270 degrees. Invasion of the deep neck musculature can be suggested on imaging if there is direct evidence of tumor extension in the paraspinal musculature.
Follow-up scanning for recurrent adenopathy after irradiation or neck dissection is a challenging but very important task. There is a growing trend to image patients prior to planned neck dissection. Recent investigations have questioned the need for planned neck dissection if there is complete radiographic resolution following combined chemotherapy and radiation therapy. Recent studies have suggested that a greater than 90% reduction in the volume of a metastatic node following combined therapy compared with a pretreatment study predicts eradication of tumor within the node (140). Film interpretation
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requires familiarity with the appearance of the neck after irradiation and the degrees of neck dissection: limited and comprehensive (141). Imaging of the postsurgical neck is even more challenging. A typical problem area is the infiltrated appearance of the high carotid sheath after dissection that included sacrifice of the jugular vein. This is an infrequent site for recurrence and such a diagnosis should be made with caution, particularly in the absence of a developing lower cranial neuropathy. Flap reconstructions must be interpreted carefully because of local distortion at the reconstructed site (Fig. 13.20) and the distortion related to the dissection for the attachment of the vascular pedicle (142,143). Usually, some degree of redundancy occurs (related to the positioning of the flap) and often gives rise to the imaging appearance of a pseudomass (see Fig. 19.9). This effect is typical on follow-up of the interposed jejunum after laryngopharyngectomy.
Figure 13.15 Metastatic squamous cancer. Serial enhanced axial computed tomography images show typical pattern of moderately enhancing pathologic lymph nodes (arrows) mixed with necrotic nodes (arrowheads) in a patient with a supraglottic primary tumor. Contrast this with the more homogeneous pattern of lymph nodes despite varied sizes in lymphoma (see Fig. 34.3).
Figure 13.16 Neck magnetic resonance imaging survey. Direct coronal T1 view (top) of posterior chain (left) and anterior chain (right) show no pathologic nodes (arrows). Coronal view also covers the tracheoesophageal grooves in the superior mediastinum (curved arrows). Selected axial T2 views of suprahyoid and infrahyoid neck confirm N0 status.
Figure 13.17 Virchow lymph node. Enhanced serial axial computed tomography images through the lower neck. A necrotic lymph node at the left venous angle (arrows) and a smaller pathologic lymph node (arrowhead) due to a clinically occult primary squamous cancer of the esophagus (curved arrow) are shown.
Figure 13.18 Serial enhanced axial computed tomography images show the value of 5-mm thick sections at the suprahyoid neck. The differential venous opacification results in the appearance of a suspicious lymph node in the anterior chain (arrow) on one section. Inspection of serial sections confirms the facial vein (arrowheads) draining into the internal jugular vein (asterisk).
Figure 13.19 False-positive lymph node staging. Enhanced axial computed tomography (top) and reformatted coronal and parasagittal views (bottom) show a lesion in the carotid space (arrows) suspected to be adenopathy. Percutaneous computed tomography-guided biopsy yielded neuroma.
Figure 13.20 Flap reconstruction. Axial T1-weighted magnetic resonance image of a reconstructed pharynx. Distortion of the tongue base (T) related to position of myocutaneous graft (G), which is applied to the carotid space (C) and prevertebral plane of the spine (S).
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