History/Classification of Nodal Levels and Neck Dissections

2 History/Classification of Nodal Levels and Neck Dissections

Angela M. Osmolak and Jesus E. Medina


The management of the cervical lymph nodes in patients with squamous cell carcinoma of the upper aero-digestive tract has evolved, since the beginning of the 20th century, along with the evolution of the neck dissection. In addition to a historical review of this evolution, this chapter presents a detailed review of two of the key elements that have driven the evolution of the radical neck dissection into several neck dissections, each of which has different indications. These elements are (1) a progressive understanding of the anatomy of the lymphatic drainage of the head and neck region and (2) clinical and histopathological observations of the patterns of lymph node metastases of cancers in the different areas of the upper aerodigestive tract and of the skin of the head and neck. The chapter concludes with a description of the different neck dissections, the nomenclature used to designate them, and the different classification systems that have been proposed to date.

Keywords: neck dissection, neck

2.1 History and Evolution of the Neck Dissection

The spread of cancer of the mouth to the “lymph glands” was mentioned in the literature as early as the mid-1800s only to point out that once this had occurred, removal of the disease and cure were not possible. A thorough historical review of surgical procedures to remove “cancer in the neck” nodes, prior to 1951, can be found in Hayes Martin’s landmark paper on “Neck dissection.”1 In this review, Martin mentions an attempt to remove “cancer of the neck with an incision from the masseter to the clavicle,” reported by Warren in 1847. He adds the comment that this operation was improvised rather than a planned procedure based on anatomical considerations. He also mentions an operation, described by Kocher in 1880, in which a tongue cancer was removed incidentally through the submaxillary triangle first, “clearing out the lymphatic glands and the sublingual and submaxillary salivary glands.” Subsequently, Kocher proposed the notion that cervical lymph nodes involved with cancer should be removed more widely, and he introduced the Y-shaped “Kocher incision.” In the literature of the latter part of the 19th century and very early in the 20th century, there were several mentions of operations to remove cancer in the cervical lymph nodes, which were in essence nonsystematic, variably extensive “extirpations” of cervical lymph nodes.

It appears that an operation first labeled as a “radical neck dissection” (RND) was performed in 1888 by a Polish surgeon by the name of Fr. Jawdinsky. In that regard, Edward Towpik, MD, PhD, wrote in the Gazeta Lekarska in 18882 (image Fig. 2.1):

Although not the first to perform the operation, Jawdynski was, to my knowledge, the first to describe the technique and extent of radical en-bloc neck dissection. Published in a Polish medical journal, his contribution remained virtually unknown abroad. Jawdynski himself was apparently not aware of the true importance of his operation; he never mentioned its potential application in removing lymph node metastases.

The first description of a systematic blocklike removal of the lymphatics of the neck for lymph node metastases was published by Crile in 1906.3 He actually attempted a complete removal of the cervical lymphatics, the sternocleidomastoid muscle (SCM), the internal jugular vein (IJV), and all of the areolar and lymphatic tissue of the various triangles of the neck. Interestingly, however, the drawings that illustrate Crile’s publication depict the spinal accessory nerve (SAN) and the ansa hypoglossi being preserved (image Fig. 2.2).

Removal of the SAN during cervical lymphadenectomy was actually advocated by Blair and Brown in 19334 as a means to decrease operating time and, more importantly, to assure a complete removal of the cervical lymph nodes. In subsequent years, other clinicians concurred with the desirability of removing the SAN.5 However, this concept was championed and popularized in the 1950s by Martin,6 who stated: “Any technique that is designed to preserve the spinal accessory nerve should be condemned unequivocally.” As Chief of the Head and Neck Surgery Service at Memorial Sloan Kettering, he was very influential at the time. His book Surgery of Head and Neck Tumors published in 1957 was a benchmark in head and neck surgery for at least a couple of decades since.6 As a result, the RND was considered for many years the only acceptable operation for the treatment of the neck in patients with cancer.

At the same time, however, the observation that resection of the SAN results in significant postoperative shoulder dysfunction prompted clinicians like Ward and Roben7 to modify the operation by preserving the SAN, whenever possible, in order to prevent postoperative shoulder drop.

In 1963, Suarez published a landmark paper entitled “El Problema de las Metastases Ganglionares y Alejadas” (The Problem of the Lymphatic and Distant Metastases).8 In it, he presented the results of a study of the lymphatics of the larynx and hypopharynx in 1,318 cases with neoplasms of these sites in whom he performed 532 therapeutic neck dissections and 271 “prophylactic” neck dissections. His observations resulted in what is, arguably, the most detailed description of the lymphatics within the larynx and hypopharynx. He noted that the lymphatic vessels are not within the fascia that envelops muscles like the SCM, do not traverse the muscles per se (instead they are located and run within the connective tissue), and they are not a part of the adventitia of neighboring veins, but are located outside of it. Suarez then described an operation that “eliminates all the areolar tissue, fascia and lymph nodes and leaves the muscles, great vessels and noble parts without mutilation.” He called it “functional dissection.” Although Suarez did not report specific outcomes, he indicated in this paper that he obtained good results with the technique he described. Nevertheless, the functional neck dissection was adopted and popularized in America and particularly in Europe, and the oncologic and functional results reported by several clinicians were excellent in the treatment of both the N0 and the N + neck. The feasibility and effectiveness of the functional neck dissection were validated by other clinicians, and this operation became the mainstay of the surgical treatment of the neck in patients with larynx cancer in Europe, South America, and, to a lesser extent, the United States.

Undoubtedly, the observations of Suarez were truly seminal and influenced open-minded clinicians at the MD Anderson Cancer Institute like Alando Ballantyne, Richard Jesse, Robert Byers, and Robert Lindberg who, in addition, noted that metastases were more likely to occur to certain lymph nodes in the neck, depending on the location of the primary tumor. These surgeons began to remove only those lymph node groups that were at highest risk of containing metastases.9

These operations were eventually called “selective neck dissections” (SNDs).10 The rationale for these neck dissections has been validated by anatomic,11 pathologic,12,13 and clinical investigations,14,15,16,17 demonstrating that cervical lymph node metastases do, indeed, occur in predictable patterns in patients with squamous cell carcinomas of the head and neck. Tumors of the oral cavity metastasize most frequently to the neck nodes in levels I, II, and III, whereas carcinomas of the oropharynx, hypopharynx, and larynx involve mainly the nodes in levels II, III, and IV. These observations coupled with the results of several retrospective and prospective clinical studies showing that, when an SND is utilized for the elective treatment of the regional lymphatics, regional control and survival rates are similar to those obtained with more extensive neck dissections16,18,19,20,21,22,23,24 were responsible for the current near universal acceptance of SND for the management of the N0 neck.

Recent studies have shown that the predictability of lymphatic spread applies to both occult (N0 neck) and clinically evident (N + neck) lymph node metastases.13,18,25 As a result, SNDs are now being used in the treatment of selected N + patients. SNDs are associated with less postoperative dysfunction of the trapezius muscle, which, when it occurs, is usually temporary and reversible.26,27,28,29,30,31 Furthermore, in the last couple of decades the role of neck dissection has evolved toward that of a staging procedure; the findings on the histopathological examination of the neck dissection specimen are now used for decision-making regarding the need for adjuvant postoperative radiation therapy32,33 and in some instances chemotherapy.34,35

2.2 Classification of Nodal Levels

The lymph nodes of the head and neck region have been designated in various ways over the years. The first fundamental nomenclature of the neck is derived from the work of Henri Rouvière. His 1932 publication, Anatomie des Lymphatiques de l’Homme, eloquently and anatomically details the 10 principal lymph node groups of the head and neck. The six groups that lie within the neck are as follows36,37:

Occipital nodes: These are nodes located at the junction of the nape of the neck and the cranial vault. They are divided into three groups: suprafascial/superficial, subfascial, and submuscular/subsplenius. The suprafascial/superficial nodes are intimately related to the third part of the occipital artery and the great occipital nerve. They are located on the posterosuperior angle of the SCM and on the fibrotendinous tissue covering the occipital bone between the insertions of the SCM and trapezius muscles. The subfascial node is located on the splenius muscle beneath the superficial layer of the deep cervical fascia, near the superior curved line of the occipital bone. The submuscular/subsplenius nodes are located beneath the splenius capitis along its superior insertion, above the obliquus capitis superior muscle and medial to the longissimus capitis muscle.

Submaxillary nodes: These nodes are located around the submaxillary gland. They are divided into five groups: preglandular, prevascular, retrovascular, retroglandular, and intracapsular. The preglandular nodes are intimately related to the submental vessels and are located in the triangular space in front of the gland, bordered by the mandible, the lateral border of the anterior belly of the digastric, and the anterior extremity of the submaxillary gland. The prevascular nodes are located on the submaxillary artery in front of the anterior facial vein. The retrovascular nodes are located behind the anterior facial vein and sometimes along the posterior border of the submaxillary gland. The retroglandular nodes are located behind the submaxillary gland and the retrovascular nodes, medial and slightly below the angle of the mandible. The intracapsular nodes lie within the capsule of the submaxillary gland.

Submental nodes: These are nodes that are located directly on the mylohyoid, in the region bordered by the mandible, the hyoid, and the anterior bellies of the digastric muscles. They are divided into three groups: anterior, middle, and posterior.

Retropharyngeal nodes: These nodes are divided into lateral and median groups. The lateral nodes are located bilaterally in the lateropharyngeal space between the posterior wall of the pharynx and the prevertebral fascia. Anteriorly, these nodes project across the superior aspect of the oropharynx onto the soft palate and palatine tonsils. Laterally, they course along the internal carotid artery near its entrance into the carotid canal and along the superior pole of the superior cervical ganglion of the sympathetics. The median nodes are located at the midline, directly on the posterior surface of the pharynx from the base of the skull to the level of the plane drawn through the extremities of the greater cornua of the hyoid bone.

Anterior cervical nodes: These nodes are located below the hyoid bone and between the two carotid sheaths. They are divided into two groups: the anterior jugular chain and the juxtavisceral chain. The anterior jugular chain nodes are located along the anterior jugular vein in the space bordered by the superficial layer of the deep cervical fascia and the SCM and the pretracheal layer of the deep cervical fascia and the infrahyoid muscles. The juxtavisceral chain nodes are located in front of the larynx and the thyroid gland and in front of and along the lateral surfaces of the trachea along the recurrent laryngeal nerves (RLN). This chain is further divided into four subgroups: prelaryngeal, prethyroid, pretracheal, and latero (para) tracheal. The prelaryngeal nodes include the interthyroid aggregation in front of the thyrohyoid membrane, the thyroid aggregation in front of the middle part of the thyroid cartilage, and the intercricothyroid aggregation in front of the cricothyroid membrane. The prethyroid nodes are located in front of the thyroid gland isthmus. The pretracheal nodes are located in front of the trachea between the inferior aspect of the thyroid gland and the innominate vein. The laterotracheal nodes are located bilaterally along the RLNs.

Lateral cervical nodes: These nodes are divided into superficial and deep groups. The superficial nodes lie along the external jugular vein (EJV) on the outer surface of the SCM. The deep nodes include the internal jugular chain, the spinal accessory chain, and the transverse cervical chain. The internal jugular chain is divided into lateral and anterior. The lateral nodes extend along the lateral border of the IJV from the posterior belly of the digastric to the junction of the IJV and the omohyoid muscle. The anterior nodes are divided into three groups: superior, middle, and inferior. The superi- or group lies between the inferior border of the posterior belly of the digastric and the thyrolinguofacial venous trunk. The middle group lies between the thyrolinguofacial venous trunk and the omohyoid muscle. The inferior group lies between the omohyoid muscle and the termination of the IJV. The spinal accessory chain extends along the SAN from the superior portion of the SCM to the deep aspect of the trapezius. The transverse cervical chain accompanies the transverse cervical artery and veins and extends from the inferior extremity of the spinal accessory chain to the jugulosubclavian junction.

Hayes Martin and George Pack also divided the lymph nodes of the head and neck into anatomic systems. In his 1951 paper, “Neck Dissection,” Martin divides the cervical lymphatics into three chains and three nodal groups. His descriptions of the submental nodal group, submaxillary nodal group, deep cervical/internal jugular chain, spinal accessory chain, and transverse cervical chain reflect those of Rouvière. He is the first, however, to separately describe the subdigastric nodal group, which includes nodes located just below the posterior belly of the digastric muscle. Additionally, he delineates three nodal groups associated with the IJV1 (image Fig. 2.3). Then in 1962, Pack and Ariel divided the lymph nodes of the head and neck into circular and vertical chains. The majority of these regions again reflect those described by Rouvière. The circular chain comprises nine regions, five of which are in the neck (image Fig. 2.4, image Fig. 2.5; Pack II). These regions include the occipital, superficial cervical, submental, submaxillary, and anterior cervical. The vertical chain includes the retropharyngeal, supraclavicular/transcervical, accessory chain, inferior deep cervical, tonsillar/jugulodigastric, and supraomohyoid nodes.38

A topographical division of the head and neck lymph nodes is first seen in the early 1970s. In his 1972 paper, “Distribution of Cervical Lymph Node Metastases from Squamous Cell Carcinoma of the Upper Respiratory and Digestive Tracts,” Lindberg divides each side of the neck into nine nodal regions based on pathophysiological mechanisms (image Fig. 2.6). These nine regions include submental, submaxillary triangle, subdigastric, midjugular, low jugular, upper posterior cervical, midposterior cervical, low posterior cervical, and supraclavicular nodes.14

Around the same time, the first papers referencing cervical metastases by five anatomical levels utilizing Roman numerals (I–V) were published. The system that was started by the Head and Neck Service at Memorial Sloan Kettering Cancer Center (MSKCC), some time after the publication of Martin’s paper, “Neck Dissection,” in 1951, defines the following levels:

Level I: Nodes within the submental and submandibular triangles.

Feb 14, 2020 | Posted by in OTOLARYNGOLOGY | Comments Off on History/Classification of Nodal Levels and Neck Dissections

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