19 Neck Dissection for Thyroid Carcinoma

Thyroid carcinoma arises from the thyroid gland, an endocrine organ located in the anterior neck responsible primarily for the regulation of body metabolism. According to Surveillance, Epidemiology, and End Results (SEER) estimates, there will be an estimated 56,870 new cases of thyroid cancer diagnosed in 2017, representing 3.4% of all new cancer cases within the United States. Most new patients are diagnosed during the fifth and sixth decades of life, with a predilection for females and the Caucasian race. The rate of new thyroid cancers has been rising on an average of 3.8% over the past 10 years, seemingly due to increased awareness and detection. Current 5-year survival rates for all comers with thyroid cancer is 98.2%, representing one of the highest survival rates among cancers.¹

There are five defined types of thyroid carcinoma: papillary thyroid carcinoma (PTC), follicular thyroid carcinoma (FTC), Hürthle cell (oncocytic), medullary thyroid carcinoma (MTC), and anaplastic. Differentiated thyroid carcinoma (DTC), papillary and follicular, makes up more than 90% of all thyroid cancers. Within DTC, papillary accounts for about 85% of cases.² PTC is known to spread primarily through the lymphatic system. This usually begins within the first echelon nodes in the central neck compartment (level VI) before spreading to the lateral neck (levels II-IV) or into the superior mediastinum (level VII). FTC, on the other hand, primarily spreads hematogenously with common local invasion of the primary tumor.

It has been established that DTC involves cervical lymph node metastases in 20 to 50% of patients. Cervical lymph node metastasis is a known risk factor for significantly predicted poorer overall survival outcomes.² MTC is categorized separately from DTC because it develops from a different cell type within the thyroid, the parafollicular C cells. It has been well established that MTC behaves more aggressively than DTC, and therefore, should be treated differently. In the sporadic type of MTC, 70% of patients who present with a palpable thyroid nodule have cervical metastases.³ Because of this high rate of metastases, MTC has a different staging system and recommendations for initial surgical treatment.

The current standard of treatment for all types of thyroid carcinoma is surgical excision in the form of hemi or total thyroidectomy with or without neck dissection at the same time. The need for surgical removal of the lymph nodes of the central and lateral neck, therefore, comes into question during the surgical planning for the treatment of thyroid cancer. Evaluation of the neck for metastases should begin with a cervical ultrasound, preferably at the time of initial diagnosis. Anatomy of the central neck compartment should be completely understood to weigh the risks and benefits of a prophylactic central neck dissection in the clinically negative neck, and to prevent complications during a therapeutic central neck dissection. Lateral neck dissection, commonly done with minimal patient morbidity, should only be done in the presence of confirmed lateral neck pathologic disease.

19.2 Preoperative Evaluation of the Neck for Thyroid Carcinoma

Once the diagnosis of thyroid carcinoma has been established, the neck needs to be evaluated for the presence of locoregional metastasis. The pattern of lymph node metastasis is somewhat predictable for all types of thyroid carcinoma based on location of the tumor within the gland, as seen in Fig. 19.1. Upper third tumors have almost a 3.3 times increased incidence of lateral neck spread (level III/IV) compared to middle or lower third tumors. Likewise, middle third and lower third tumors have about a 3 to 13.5 times increased incidence of central neck spread (level VI/VII) compared to upper third tumors.⁴ Initial screening of the central and lateral neck compartments of all patients should be done via cervical ultrasound followed by additional imaging studies (usually CT) for advanced, bulky, or invasive disease.²

If, after physical examination and preoperative imaging studies, the patient does not have pathologic appearing lymph nodes, they are classified as a clinically negative neck (cN0). Any lymphadenopathy found should be further investigated. The most common way to diagnose suspicious thyroid nodules and lymph nodes is to perform ultrasound-guided fine needle aspiration (USGFNA). In a high-volume, multispecialty center, FNA can be performed and interpreted by a pathologist during the same clinic visit, expediting the diagnosis, surgical planning, and initiation of treatment. Incisional biopsy is not recommended because this commonly requires entering into or near the thyroid, causing scarring and possibly increasing the difficulty of the subsequent thyroidectomy and/or neck dissection. Once metastasis has been confirmed in either the central or lateral neck, the patient is classified as a clinically positive neck (cN1a or cN1b, respectively).

Fig. 19.1 Lymphatic drainage of the thyroid gland. Superior third tumors have a higher propensity to spread to the lateral neck compared to middle and lower third tumors, which tend to metastasize to the central neck first. (Reproduced from Tang AL, Steward DL. Developmental and surgical anatomy of the thyroid compartment. In: Terris DJ, Duke WS, eds. Thyroid and Parathyroid Diseases: Medical and Surgical Management. New York, NY: Thieme; 2016:11.)

Cervical ultrasound of the central and lateral neck should be completed at the time of initial evaluation and FNA of suspected thyroid carcinoma. Preoperative ultrasound identifies suspicious cervical adenopathy in 20 to 31% of cases. Features suspicious for metastatic cancer involvement include enlargement, loss of fatty hilum, round shape, hyperechogenicity, cystic changes, microcalcifications, and increased peripheral vascularity.² No single feature is absolute for malignancy; so, the decision to perform an FNA should be based on the totality of patient risk factors, imaging characteristics, and size greater than 10 mm.

If initial evaluation of an FNA from a lymph node is indeterminate (Bethesda class II), thyroglobulin washout can be completed on the specimen. The addition of thyroglobulin washout is helpful in lymph nodes which are cystic, inadequate, or have indeterminate cytologic evaluation, or inconsistent sonographic characteristics. Currently, studies show that a thyroglobulin level less than 1 ng/mL indicates a benign node.² No level has been established to indicate malignancy and current research into the ratios of FNA thyroglobulin to serum thyroglobulin may increase predictive accuracy.⁵

19.2.2 Additional Imaging

The American Thyroid Association (ATA) advocates for the use of cervical ultrasound as the first-line imaging for evaluation of nodal metastasis, followed by cross-sectional imaging such as computed tomography (CT) or magnetic resonance imaging (MRI) if needed. Indications for further imaging would include invasive primary tumor, advanced disease, inability to fully assess nodal extent on ultrasound, posterior location of the thyroid tumor (adjacent to trachea or esophagus), and multiple or bulky lymph node involvement. Invasive disease can be clinically evident with hoarseness, shortness of breath, dysphagia, hemoptysis, or airway obstruction. Findings consistent with laryngeal, tracheal, and/or esophageal involvement will prompt the surgeon to prepare accordingly.

19.2.3 TNM and Staging

The most commonly used staging system for thyroid cancer was developed by the American Joint Committee on Cancer (AJCC). Unlike other cancers of the head and neck, age is an important prognostic factor in this staging system. There are also separate classifications for differentiated, medullary, and anaplastic histologic diagnoses. Table 19.1 and Table 19.2 outline the 7th edition of the AJCC classification for differentiated and medullary thyroid cancer, respectively. Updates to the classification system are expected to take effect in the near future, with the most significant change being increasing the age of poorer prognosis from 45 to 55 years of age. Furthermore, after further studies on survivability, the stages have been shifted down, requiring more advanced disease for higher classification.

19.3 The Central Neck

19.3.1 Surgical Definition of Central Neck Levels

Effective communication of preoperative planning, intraoperative dissection, pathologic reporting, and administration of adjuvant treatment is based on the uniformity of terminology by defining the relevant anatomy of the central neck compartment. Collaboration of multiple surgical societies has led to the definition of the central neck compartment and how it relates to thyroid surgery. The central neck compartment can be defined as levels VI and VII and shown in Fig. 19.2, and includes all of the neurovascular, lymphatic, and visceral components contained within its boundaries.^6,7

Table 19.1 American Joint Committee on Cancer TMN Classification for Differentiated and Medullary Thyroid Cancer.

Fig. 19.2 Anatomical neck levels. The central neck compartment is defined as levels VI and VII. The lateral neck compartment is defined as levels I through V. (Reproduced with permission from Genden EM, Kao J, Packer SH, Jacobson AS. Carcinoma of unknown primary site. In: Genden EM, Varvares MA, eds. Head and Neck Cancer: An Evidence-Based Team Approach. New York, NY: Thieme; 2008:181.)

The level VI compartment is bounded superiorly by the inferior border of the hyoid bone, laterally by the medial border of the carotid arteries, anteriorly by the superficial layer of the deep cervical fascia, posteriorly by the deep layer of the deep cervical fascia, and inferiorly by the plane of the sternal notch. The level VII compartment, or anterior superior mediastinal compartment, is bounded superiorly by the plane of the sternal notch, laterally by the mediastinal pleura, anteriorly by the posterior border of the manubrium, posteriorly by the deep layer of the deep cervical fascia, and inferiorly by the innominate artery on the right and corresponding axial plane on the left.⁷

Lymph Nodes

Within the central neck compartment, the lymph node groups are further defined based on location. The prelaryngeal, or Delphian, nodes are located anterior to the thyroid cartilage and superior to the thyroid gland. The pretracheal nodes are located anterior to the tracheal and between the thyroid gland and the sternal notch. The right and left paratracheal nodal groups are located on either side of the trachea, but have important differences based on the course of their respective recurrent laryngeal nerves (RLNs). In the left paratracheal region, lymphatic tissues generally lie anterior to the RLN. However, since the right RLN courses more ventrally within the paratracheal region because of the innominate artery, lymphatic tissue lies both anterior and posterior to the nerve. Bilaterally, the remaining borders of the paratracheal region are the trachea medially, the common carotid artery laterally, and the retropharyngeal and retroesophageal regions posteriorly.⁷

Vascular Structures

As described earlier, many vascular structures are present in the central neck compartment. The surgeon needs to be aware not only these vessels but also of their branching vessels. The brachiocephalic, or innominate artery, is the first branch of the arch of the aorta and gives rise to the right subclavian and common carotid arteries. It also determines the more ventral and lateral course of the right RLN. The left common carotid artery is the second branch of the arch of the aorta and defines the left lateral border of the central compartment. The superior thyroid artery is commonly the first branch of the external carotid artery and supplies the superior pole of the ipsilateral thyroid lobe. The inferior thyroid artery is a branch of the thyrocervical trunk from the subclavian artery and supplies the inferior pole of the ipsilateral thyroid lobe. It also supplies the ipsilateral inferior and superior parathyroid glands. The inferior thyroid artery travels posterior to the common carotid artery, but has a highly variable relationship with the RLN.⁸

The superior and middle thyroid veins drain into the internal jugular vein. The superior vein accompanies its paired artery; however, the middle vein does not have a paired artery. The inferior thyroid veins are variable in number and location, draining most commonly into the brachiocephalic veins, and also into the internal jugular vein. Although the internal jugular vein does not by definition lie in the central neck compartment, it is worth noting that its intimate association with the common carotid artery can bring it into the surgical field if tissue is dissected and retracted into the surgical field.

Nerves

Several nerves lie within the central neck compartment and have significant clinical importance. The RLN is a branch of the tenth cranial nerve (Vagus) and is derived from the sixth branchial arch. It innervates all of the intrinsic muscles of the larynx with the exception of the cricothyroid muscle and provides sensation to the larynx below the glottis, along with portions of the trachea and esophagus. During embryologic development, the RLN courses around the arteries of the sixth branchial arch. On the left, this is the ductus arteriosus, which ex utero becomes the ligamentum arteriosum. On the right, the sixth branchial artery is obliterated. The RLN then migrates cranial to the next remaining branchial artery, the right subclavian artery. Therefore, the course of the RLN varies between the right and left sides of the body.

The right subclavian artery lies more anterior and lateral compared to the aortic arch and ligamentum arteriosum on the left. This results in the nerve traveling more lateral to medial and anterior to posterior on the right when it comes back to the larynx, as opposed to simply traveling superior in the tracheoesophageal groove as it on the left. The motor fibers of the nerve enter the larynx posterior to the cricothyroid joint underneath the inferior constrictor muscle.

Although rare, the head and neck surgeon must be aware of the possibility of a non-RLN (NRLN). This anomaly occurs almost exclusively on the right, with a prevalence of 0.7% in the general population. The most common cause of an NRLN is failure of the embryologic development of the right fourth branchial arch, the subclavian artery. It has been found that 86.7% of right NRLNs are associated with an aberrant subclavian artery pattern. These nerves can originate either above or below the laryngotracheal junction and track with the superior thyroid artery, branch directly off the Vagus, or display a looping trajectory into the laryngotracheal junction.⁹

The external branch of the superior laryngeal nerve (EBSLN) branches from the Vagus nerve high in the neck and accompanies the superior thyroid vasculature as it courses toward the cricothyroid muscle. It inserts directly into the muscles, which acts as a laryngeal tensor. Classification schemes have been proposed to describe the location of the EBSLN for better identification and preservation during thyroid or central neck dissection. They focus on several aspects of the nerve’s course, including the intersection with the superior thyroid vessels, location on the nerve above a horizontal plane of the superior border of the superior thyroid pole, location of the cricothyroid–inferior constriction junction, and distance between the nerve and the superior thyroid vessels.^{10,11,12,13,14} Complete discussion of these schemes is beyond the scope of this chapter.

Parathyroid Glands

The parathyroid glands are endocrine glands located on the posterior aspect of the thyroid gland and secrete parathyroid hormone, which regulates calcium homeostasis in the circulation. The inferior parathyroid glands migrate caudally in the anterior neck in association with the thymus gland. The final location of the inferior parathyroid glands is wherever the glands separate from the thymus. This can be anywhere from the hyoid bone to the lower mediastinum. In approximately 50% of patients, the inferior parathyroid glands can be found within 1 cm inferior, lateral, or posterior to the inferior pole of the thyroid. They are located typically anterior to the coronal plane drawn along the vertical axis of the RLN.

The superior parathyroid glands migrate attached to the posterior midportion of the thyroid lobe and, therefore, have a more predictable location in the central neck. In 85% of cases, the superior gland may be located on the posterior aspect of the thyroid lobe in a 2-cm diameter circle centered 1 cm above the crossing of the inferior thyroid artery and the RLN. The superior parathyroid glands lie posterior to the coronal plane drawn along the RLN.¹⁵

19.3.2 Central Neck Dissection

In patients diagnosed with PTC, 35% present with clinically evident regional nodal metastasis. Furthermore, up to 80% of patients presenting with no clinical evidence of nodal disease will have microscopic evidence of metastasis following elective neck dissection.¹⁶ Zhang et al found in a retrospective study of more than 1,000 patients that male gender, age younger than 45 years, multifocal lesions, extrathyroidal extension, and primary tumors greater than 6 mm were risk factors for central neck metastasis.⁴

Uniformity in the reporting of nodal regions dissected, the surgical procedure performed, and the exact location of disease is crucial for the complete treatment of thyroid carcinoma. The American Head and Neck Society Endocrine Committee recently published guidelines for reporting central neck dissections. The procedure should be defined as either prophylactic (elective) or therapeutic. Distinguishing the differences between these two categories is important for the preoperative counseling of the patient. For prophylactic neck dissections, the surgeon must explain the risk, benefits, and alternatives to patients as well as why, if they have no apparent disease within the lymph nodes, he or she would advise for the removal of the lymph nodes.

Defining the extent of the central neck dissection is important for staging, adjuvant treatment, and, if necessary, revision operations. The term “central neck dissection” implies the surgeon removed the entire contents of the pretracheal and prelaryngeal lymph nodes, which is rarely the case in practice. The designation of the procedure is completed by including laterality or bilateral. By including right, left, or bilateral, the surgeon indicates removing the paratracheal lymph nodes on that respective side. Therefore, a complete description of a central neck dissection should be [prophylactic/therapeutic] [right/left/bilateral] central neck dissection.¹⁶

Complete dissection and removal of compartmental lymph nodes provide the best initial surgical management of disease. Previous methods of “berry picking,” or choosing pathologic appearing lymph nodes intraoperatively, can miss microscopic disease within the remaining lymph nodes. It can also lead to increased complications from inadequate dissection of critical structures. Therefore, berry picking lymph nodes is not recommended for central neck dissections.¹⁶

19.3.3 Prophylactic Central Neck Dissection

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