neck dissection: current concepts and future...

Surg Oncol Clin N Am 13 (2004) 151–166

Neck dissection: current conceptsand future directions

Nestor R. Rigual, MD, FACSa,b,*,Sam M. Wiseman, MD, FRCS(C)c,1

aSchool of Medical and Biological Sciences, State University of New York at Buffalo,

Buffalo, NY 14263, USAbSection of Plastic and Reconstructive Surgery, Department of Head and Neck Surgery,

Roswell Park Cancer Institute, Elm and Carlton Streets, Buffalo, NY 14263, USAcDepartment of Surgical Oncology, Roswell Park Cancer Institute, Elm and Carlton Streets,

Buffalo, NY 14263, USA

This article discusses the classification, rationale, and future directionspertaining to neck dissections in the management of cancers of the head andneck. Most head and neck cancers arise from the squamous epithelium ofthe upper aerodigestive tract. In this article, the term ‘‘head and neckcancer’’ refers to squamous cell carcinoma (SCC) of the upper aerodigestivetract.

The development of lymph node metastasis is a critical factor in guidingthe treatment and determining the prognosis of individuals diagnosed withhead and neck carcinoma. The presence of lymphatic metastases is asso-ciated with a decrease in the survival rate of up to 50% of patients [1,2].Radical neck dissection (RND), first described by Crile [3] in 1906, andpopularized by Martin et al [4], has remained the cornerstone of the surgicaltreatment of cervical lymph node metastasis throughout most of the 20thcentury. The classic RND requires en bloc resection of the cervical lymphnodes, internal jugular vein, sternocleidomastoid muscle (SCM), and spi-nal accessory nerve. This operative procedure has significant long-termmorbidity, including shoulder dysfunction, cosmetic deformity, cutaneousparesthesia, and chronic neck and shoulder pain syndrome. These morbid-ities are exacerbated when postoperative radiotherapy is added. For thesereasons, and because of a lack of rationale for removing all cervical lymph

1 Current address: Department of Surgery, St. Paul’s Hospital, 1081 Burrard Street,

Vancouver, British Columbia, Canada, V6Z 1Y6.

* Corresponding author.

E-mail address: [email protected] (N.R. Rigual).

1055-3207/04/$ - see front matter � 2004 Elsevier Inc. All rights reserved.

doi:10.1016/S1055-3207(03)00119-4

mailto:[email protected]

152 N.R. Rigual, S.M. Wiseman / Surg Oncol Clin N Am 13 (2004) 151–166

nodes, a change in the surgical approach to managing cervical metastasiswas initiated by Suarez [5] in the late 1950s. In anatomic studies, Suarezdemonstrated that cervical lymphatics are contained within well-definedfascial compartments, separate from muscles, nerves, blood vessels, andother visceral structures of the neck. Thus, he proposed that muscles, bloodvessels, and nerves that were routinely removed during an RND could bepreserved without compromising regional disease control in patients whohad limited neck disease. Bocca et al [6] subsequently popularized this‘‘functional neck dissection’’ concept, or neck dissection with the pre-servation of vital structures. The development of a better understanding oflymph node drainage patterns [7,8], the discovery of fascial compartmentsseparating cervical lymph nodes from neck structures commonly removed inRND, and an improved understanding of the role of adjuvant radiationtherapy [9,10] have been the impetus for the development of current modi-fications of the RND.

In response to a need for an organized approach for describing andclassifying neck dissection, the Committee for Head and Neck Surgery andOncology of the American Academy of Otolaryngology/Head and NeckSurgery standardized neck dissection terminology in 1991 [11], and a morerecent update was published in 2002 [12]. Neck dissection classificationcategories are shown in Box 1.

In the current classification schema, the location of cervical lymph nodegroups is delineated by the level system [11]. This system is easy to rememberand has become widely accepted (Fig. 1).

Recently, the concept of neck sublevels has been introduced into theclassification schema, because areas have been identified within the six necklevels that seem to have independent oncologic significance [12]. Thesesublevels include level IA (submental nodes), level IB (submandibularnodes), levels IIA and B (upper jugular nodes), level VA (spinal accessorynodes), and level VB (supraclavicular nodes). The lymph node groupscontained in these levels and the anatomic boundaries of the six neck levelsare shown in Table 1. Lymph node groups not located within these regionsshould be referred to by their specific nodal group name. Examples includeretropharyngeal, periparotid, and suboccipital nodal groups.

The structures defining the anatomic boundaries of the neck levels andsublevels are depicted in Fig. 2. Most of these anatomic boundaries are

Box 1. Neck dissection classification

� Radical neck dissection� Modified radical neck dissection� Selective neck dissection� Extended neck dissection

153N.R. Rigual, S.M. Wiseman / Surg Oncol Clin N Am 13 (2004) 151–166

familiar and well-defined anatomic structures, with few exceptions. Theposterior boundary of levels II through IV is delineated by the posteriorborder of the SCM or by the sensory branches of the cervical plexus. Thesecervical plexus sensory nerve branches also define the anterior boundary oflevel V. The anterior border of level IIA is defined by the stylohyoid muscle(see Table 1).

Imaging-based classification of cervical lymph node groups

Imaging studies were not used in the initial neck dissection classificationscheme in 1991 [11].

Radiologists therefore have recently identified landmarks that accuratelydefine the location of lymph nodes and have devised an imaging-basedclassification scheme for the cervical lymph node groups [13]. Thisradiologic classification was designed as an adjunct to the clinically basednodal classifications. Using imaging landmarks, level IA includes the lymphnodes that are located between the medial margin of the anterior belly ofthe digastric muscles, superior to the body of the hyoid bone, and belowthe mylohyoid muscle. Level IB includes nodes that also lie below the

Fig. 1. The levels of the neck. (Drawing by Paul Tomljanovich, MD, medical illustrator.)

Table 1

Neck level ana

Level Sup edial (anterior) Lateral (posterior)

IA Ma ontralateral digastric muscle,

anterior belly

Ipsilateral digastric muscle,

anterior belly

IB Ma nterior belly of digastric

muscle

Stylohyoid muscle

IIA Bas tylohyoid muscle Plane (vertical) defined by

spinal accessory nerve

IIB Bas lane (vertical) defined by

spinal accessory nerve

Sternocleidomastoid muscle,

lateral border

III Pla

d

o

ternohyoid muscle,

lateral border


lateral border, or cervical

plexus sensory branches

IV Pla

b

c

ternohyoid muscle, lateral

border


lateral border, or cervical


VA Ap

o

s

ternocleidomastoid muscle,

posterior border, or cervical


Trapezius muscle,

anterior border

VB Pla

in

o

ternocleidomastoid muscle,

posterior border, or cervical


Trapezius muscle,

anterior border

VI Hy ommon carotid artery Common carotid artery

154

N.R.Rigual,S.M

.Wisem

an/Surg

OncolClin

NAm

13(2004)151–166

tomic landmarks

erior Inferior M

ndibular symphysis Hyoid bone body C

ndibular body Posterior belly of digastric

muscle

A

e of skull Plane (horizontal) defined by

inferior border of hyoid bone

S

e of skull Plane (horizontal) defined by

inferior border of hyoid bone

P

ne (horizontal)

efined by inferior border

f body of hyoid

Plane (horizontal) defined by

inferior border of cricoid

cartilage

S

ne (horizontal) defined

y inferior border of cricoid

artilage

Clavicle S

ex of the point of convergence

f the trapezius and

ternocleidomastoid muscles

Plane (horizontal) defined

by inferior aspect

of cricoid cartilage

S

ne (horizontal) defined by

ferior border

f cricoid cartilage

Clavicle S

oid bone Sternum C


mylohyoid muscle and above the hyoid bone but are posterior and lateral tothe anterior belly of the digastric muscles and anterior to the posteriorborder of the submandibular gland. Level II nodes are contained in thespace defined superiorly by the skull base, inferiorly by the hyoid bone,anteriorly by the posterior border of the submandibular gland, andposterior to a transverse line drawn on each axial image through theposterior edge of the SCM. The deep border of level II is defined by theinternal carotid artery in that any nodes lying medially to this vessel areconsidered to belong to the retropharyngeal nodal group. Level III nodesare located between the lower border of the hyoid bone and the lowermargin of the cricoid cartilage. These nodes lie laterally to the commoncarotid artery. On both sides of the neck, the medial margin of the carotidarteries separates the level III nodes, which are located laterally to level IVnodes, which lie medially to the vessels. Level IV nodes lie inferiorly to thelower border of the cricoid cartilage and superiorly to the clavicle. Theboundaries of levels V and VI are the same as in the clinical classification.

Neck dissection classification

The neck dissection classification system has arisen because radical neckdissection remains the standard procedure for cervical lymphadenectomy,

Fig. 2. The sublevels of the neck. (Drawing by Paul Tomljanovich, MD, medical illustrator.)


with other operations representing alterations of this classic operation (seeBox 1). The term ‘‘modified radical neck dissection’’ (mRND) is used whenone or more nonlymphatic structures routinely removed in an RND ispreserved. In general, currently preserved structures include the SCM, theaccessory nerve, and the internal jugular vein. If one or more lymph nodelevels that are routinely removed in an RND are preserved, the procedure istermed a ‘‘selective neck dissection’’ (SND). Finally, if the procedure includesremoval of additional nonlymphatic structures or lymph node groups(relative to the RND), the operation is termed an ‘‘extended neck dissection.’’

The anatomic boundaries of the RND include the following: superiorly,the inferior border of the mandible; inferiorly, the clavicle; medially, themidline; and posteriorly, the anterior border of the trapeziusmuscle. Includedwithin these boundaries are lymph node levels I through V, the SCM, theinternal jugular vein (IJ), and accessory spinal nerve (cranial nerve XI), whichare removed at surgery (Fig. 3).

An mRND refers to the removal of lymph node levels I through V, withpreservation of one or more nonlymphatic structures that are routinelyremoved during the course of an RND. In describing an mRND, theanatomic structure or structures preserved should be clearly specified (eg,mRND with preservation of the internal jugular vein).

SNDs are commonly used in the staging and treatment of the clinicallyundetectable (or N0) neck tumor. In this type of neck dissection, one or

Fig. 3. Radical neck dissection. (Drawing by Paul Tomljanovich, MD, medical illustrator.)


more lymph node levels are preserved. The lymph node levels removedare based on the location of the primary tumor because the clinicalpatterns of cervical lymphatic metastasis from head and neck tumors havebeen shown to be predictable in multiple, large-scale, retrospective studies[8,14,15].

The lymph nodes at risk for laryngeal, hypopharyngeal, and oropharyn-geal carcinomas are usually found within levels II, III, and IV. For thyroidcancer and subglottic cancers, the nodes in level VI are at greatest risk ofharboring metastatic disease. Lymph nodes in levels I, II, and III are atgreatest risk of harboring microscopic metastatic disease in patients whohave oral cavity primary cancers. Skip metastasis to level IV may potentiallyrepresent a problem in patients who have oral tongue carcinoma [16].

The most significant paradigm shift in the management of cervical lymphnode disease over the past decade has been the selective removal of lymphnode groups that are at greatest risk of harboring metastases. Although thischange in treatment philosophy has been applied mostly to patients with N0nodal disease, SND also has a role in the treatment of N-positive necktumors [17,18].

Selective neck dissection for oropharyngeal, laryngeal,

and hypopharyngeal cancer

The lymphadenectomy of choice in the treatment of cancers affectingthese anatomic sites includes the removal of lymph node groups in levels II,III, and IV (SND II–IV). Patients who have SCC of the larynx rarelypresent with metastases at the submandibular triangle (level I) [19]. Datafrom two recent studies support the use of SND II–IV for the treatmentof N0 laryngeal and hypopharyngeal carcinomas [20] and transglotticcarcinomas (supraglottic tumors that cross the laryngeal ventricle andinvade the glottis) [21]. The anatomic limits of this lymphadenectomy are asfollows: the clavicle inferiorly, the skull base superiorly, the lateral border ofthe sternohyoid muscle medially, and the posterior border of the SCM andcutaneous sensory branches of the cervical plexus posteriorly (Fig. 4).

With the exception of the glottic larynx, cancers of the oropharynx,hypopharynx, and larynx have bilateral lymphatic drainage patterns. Thus,the procedure of choice for patients withN0 primary tumors in these locationsis a bilateral SND II–IV in cases where the neck is managed surgically. Incancers involving the walls of the hypopharynx and oropharynx, theretropharyngeal nodes may harbor metastatic disease. Therefore, in thiscircumstance, removal of this nodal group should be considered. Theprocedure would be termed SND II–IV, retropharyngeal nodes. In laryngealand hypopharyngeal carcinomas extending below the glottic larynx, level VIlymph nodes are usually included in the neck dissection (SND II–IV, VI),because they are at risk [21].


Selective neck dissection for cancer of the oral cavity

In oral cavity cancer, the nodal groups at risk are located in levels I, II,and III [8]. The procedure of choice is SND I–III (Fig. 5). Some evidencesuggests that, in cancer of the anterior tongue, level IV nodes may containmetastatic disease [16]. Therefore, it is recommended that lymph nodes inlevel IV be removed in patients who have cancer of the tongue (Fig. 6). Incancers involving midline structures, including the floor of the mouth, theindicated procedure is a bilateral SND I–III, because the lymph nodes onboth sides of the neck are at risk for containing metastases. The adequacyof SND I–III for treating clinically negative neck tumors in patients whohave oral carcinomas has been examined thoroughly [9,10,22]. In addition,investigators have demonstrated that, in patients with pathologically posi-tive lymph nodes, the addition of postoperative radiotherapy following SNDI–III can achieve regional control comparable to that of level I–V dissectionand postoperative radiotherapy [9].

Anterior neck dissection (selective neck dissection VI)

Level VI, central compartment neck dissection refers to the removal ofbilateral, paratracheal, delphian, and perithyroiidal lymph nodes, including

Fig. 4. Selective neck dissection II–IV. (Drawing by Paul Tomljanovich, MD, medical

illustrator.)


Fig. 5. Selective neck dissection I–III. (Drawing by Paul Tomljanovich, MD, medical

illustrator.)

Fig. 6. Selective neck dissection I–IV for oral tongue cancer. (Drawing by Paul Tomljanovich,

MD, medical illustrator.)


nodes adjacent to the recurrent laryngeal nerves [7]. The superior boundaryof the dissection is the body of the hyoid bone, and the inferior margin is thesuprasternal notch. The lateral margins are defined by the common carotidarteries. SND VI is most commonly indicated in the treatment of thyroidcancer, advanced laryngeal cancer with subglottic extension, and cervicalesophageal carcinoma (Fig. 7). In thyroid cancer where there is clinicalevidence of nodal metastases in the neck, either preoperatively orintraoperatively, the procedure of choice also would include levels II to V,and is designated SND II–VI.

Extended neck dissection

Extended neck dissection is by definition more extensive than an RND.Extended neck dissection involves the removal of additional lymph nodegroups or nonlymphatic structures not included in an RND. The anatomicstructures and lymph node groups removed during the course of this oper-ation must be documented. Examples of such lymph node groups includethe retropharyngeal, suboccipital, and paratracheal nodes. Examples ofnonlymphatic structures that may be removed include the vagus nerve,carotid artery, and the strap muscle (Fig. 8).

Fig. 7. Selective neck dissection VI, or central compartment neck dissection. (Drawing by Paul

Tomljanovich, MD, medical illustrator.)


Posterolateral neck dissection

Posterolateral neck dissection is an SND that involves removal of thesuboccipital lymph nodes, postauricular lymph nodes, and lymph nodes inlevels II through V (Fig. 9). SND II–V (postauricular, suboccipital) is theprocedure of choice to treat the neck in patients with cutaneous carcinomasof the posterior scalp and neck [23].

The superior limit of the dissection is the base of skull and the nuchalline. The inferior limit of the dissection is the clavicle. The anterior (medial)limit of the dissection is the lateral border of the sternohyoid muscle. Thelateral (posterior) limit is the anterior border of the trapezius muscleinferiorly and the midline of the neck superiorly [24,25].

Sentinel lymph node biopsy: a new paradigm for staging N0 neck tumors

Sentinel lymph node biopsy (SLNBX) has become an accepted techniquefor staging the first extratumoral echelon of draining lymph nodes inindividuals diagnosed with melanoma or breast cancer. Similar to SND,SLNBX is based on the principle that lymphatic metastases do not occur ina random manner, but rather predictably, in accordance with preexistinglymphatic anatomy. As discussed, the practice of Staging SND, performed

Fig. 8. Extended neck dissection (common carotid artery, digastric muscle, hypoglossal nerve).

(Drawing by Paul Tomljanovich, MD, medical illustrator.)


by removing nodal levels with the highest probability of harboring metastaticdisease, is based on studies examining the pattern and incidence of metastasesin large patient cohorts. Unlike SND, however, SLNBX is a lymphaticmapping technique that allows for the direct evaluation of the lymph node ornodes that initially receives metastatic disease, in a specific individual, witha tumor at a specific location.

Patients who have N0 head and neck cancer may benefit most fromSLNBX. Approximately 20% to 40% of patients who have N0 diseaseharbor microscopic tumor foci [26–28]. Thus, approximately two thirds ofpatients who have N0 head and neck cancer will have no pathologicevidence of metastatic disease [26,29]. Taking a ‘‘wait and see’’ approach inpatients with N0 cancer has been associated with disease recurrence anda worsened prognosis [26]. SLNBX has the potential of avoiding eitherovertreatment or undertreatment of the neck. In addition, SLNBX has theadded benefit of improved disease staging by directing the pathologist to the‘‘highest risk’’ lymph node or nodes, which may be more extensively eval-uated by either immunohistochemical or molecular techniques. Hamakawaet al [30] determined that routine histologic evaluation of neck dissectionspecimens miss micrometastatic disease in up to 28% of patients. It is thisgroup of ‘‘understaged’’ patients with head and neck cancer that may espe-cially benefit from SLNBX.

Recently, Wiseman et al [31] presented the results of a pilot study usingan isosulfan blue dye technique to carry out SLNBX in patients with early-

Fig. 9. Selective neck dissection II–V (postauricular, suboccipital), or posterolateral neck

dissection. (Drawing by Paul Tomljanovich, MD, medical illustrator.)


stage N0 oral cavity head and neck cancer. Although SLNBX wastechnically feasible, and no adverse effects were observed in the authors’patient population, the sentinel node identification rate was only 57%, andwhen identified, the sentinel node accurately predicted the pathologic statusof the neck in 75% of patients. The negative predictive value for the absenceof cervical metastases was 67% [31]. The authors’ experience was similarto that of other investigators who found that a vital dye technique alonehad a low rate of sentinel node identification (0%–67%), and even whenidentified, the sentinel node often did not accurately predict the pathologicstatus of the neck (0%–75%) [32,33]. The poor clinical utility of the vitaldye methodology is a sharp contrast to the high rate of sentinel nodeidentification reported when a radiotracer technique is used (in most series,100% of sentinel nodes were identified) [34–44]. In addition, using theradiotracer technique, the sentinel node almost always accurately reflectedthe pathologic status of the neck. Other investigators have used a combinedvital dye/radiotracer technique and have reported that these methodologiescomplement one another and also have high rates of sentinel node iden-tification (90%–100%) and accurate nodal staging (97%–100%) [43–45].

Recently, Ross et al [46] reported pooled results, from 22 centers, ofSLNBX being performed on 316 patients who had N0 head and neckcancer. Although this study was not prospective, and the study populationwas treated heterogeneously, these investigators reported a 95% rate ofsentinel node identification and an overall sensitivity of 90% for thisprocedure. At centers that performed 10 or fewer procedures, the sensitivitywas 57%; centers that performed more than 10 procedures had a sensitivityof 92% [46].

Although the data reported by Ross et al [46] are provocative, they mustbe interpreted with caution because this study was performed in a patientcohort that was nonrandomized, uncontrolled, retrospectively collected, andheterogeneous. The results reported in the current literature are encourag-ing, however. SLNBX does seem to be a technically feasible and accuratemethod for staging N0 neck cancer. There remain many issues that mustbe addressed before SLNBX becomes integrated into the managementalgorithm of N0 neck cancer. Critical unresolved issues include the identi-fication of patient/tumor characteristics appropriate for this methodology(eg, stage, site, subsite) and a determination of the technique (eg, radio-tracer, vital dye, or combination technique) most appropriately applied tothese individuals.

Summary

For individuals diagnosed with head and neck cancer, neck dissectionmay be performed for therapy or disease staging. The classification of neckdissection and the definition of precise anatomic landmarks have allowed


for this operation, and its many variations, to become standardized world-wide. SLNBX shows promise in its ability to accurately stage N0 head andneck cancer and may allow patients with no micrometastatic disease toavoid neck dissection. Before this technique becomes adopted into routineclinical practice, however, it must first be prospectively scrutinized in largepatient populations. Regardless of the future role of SLNBX in the man-agement of head and neck cancer, currently it is only through a completeunderstanding of the clinical, theoretic, and technical aspects of neck dis-section that surgeons may benefit individual patients and the head and neckcancer patient population as a whole.

Acknowledgment

The authors thank Paul Tomljanovich, MD, for his excellent artwork.

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