Werner & Ingbar's The Thyroid: A Fundamental & Clinical Text, 9th Edition

17.Surgical Anatomy

Robert M. Beazley

HISTORY

An understanding of the embryology and anatomy of the thyroid gland is important in both the medical and surgical management of thyroid diseases. In the former, it is critical to interpreting diagnostic studies especially ultrasound (US), nuclear, magnetic resonance image (MRI), and computed tomography scans (CT). In the latter case, the requirement is self-evident, with the best surgical results occurring in the hands of those individuals with an extensive and complete understanding and appreciation of the anatomy of the thyroid. Indeed, the great surgeon Halsted said “the extirpation of the thyroid gland for goiter typifies better than any operation the supreme triumph of the surgeon's art” (1).

Anatomical manifestations of the abnormal thyroid gland were recognized centuries before the gland itself was described. Goiters were first appreciated in China in 2700 B.C., while 300 years later the Romans recognized endemic goiters in the Alps. In the 7th century A.D., Paul of Aegina is reported to have been the first physician to describe a goiter, which he called a “bronchocele.” Albucasis, the great Arabian physician, remarked on “the elephant of the throat” seen in women in the 11th century. Leonardo da Vinci sketched a bilobed structure he observed in the neck around 1500. Vesalius's great anatomical work De Fabrica Humani Corporis (1543) illustrates two “glandulae larynges,” which he postulated functioned to lubricate the larynx. Although the Roman Bartholomaeus Eustachius (1520–1574), discoverer of the “adrenal glands,” described a single glandulam thyroideum, with an isthmus connecting the lobes, his work was not published until the 18th century. Thomas Wharton (1614–1673) of London described the “glandula thyroidoeis,” naming it because of its relationship to the thyroid cartilage. Fred erick Ruysch of Leiden utilized the microscope in 1750 to reveal the vesicles in the thyroid gland.

Thyroid surgery did not come of age until the seventh decade of the 19th century, although sporadic attempts at surgical manipulation were recorded in Europe and America between 1596 and 1848, largely with disastrous results. Indeed, the evolution of thyroid surgery is the paradigm of modern surgery. Billroth (1829–1894) and Kocher (1841–1917) in Europe and Charles Mayo (1866–1939), William Halsted (1852–1922), and George Crile (1864–1943) in America were prominent contributors to the evolution of thyroid surgery. In his classic review “The Operative Story of Goiter,” Halsted stated that the operation had become “essentially perfected in Switzerland, Germany and Austria by 1883” (1). Interestingly, the major technical details of thyroidectomy have changed very little in the last 125 years.

EMBRYOLOGY

Thyroid Gland

A thorough understanding of the embryologic development of the thyroid is the key to understanding surgical anatomy. Initial thyroid development is discernible around the third week with appearance, at the level of the second branchial arch, of a median anlage on the ventral pharyngeal wall. Invagination of this midline thickening evolves as a single or paired diverticulum, which migrates caudally toward the base of the neck to become the lateral thyroid lobes. In the developed fetus, the origin of the median anlage is recognized as the “foramen cecum.” A stalk of degenerating follicular cells connects the invaginated median anlage to the foramen cecum, thus forming the thyroglossal duct. By the fifth week, the thyroglossal duct is markedly attenuated and begins to break into fragments, disappearing in most cases by the eighth week. Also, around the fifth week the lateral thyroid anlage, having developed from the ventral portion of the fourth pharyngeal pouch, originates and fuses to the posterior aspect of the lateral thyroid lobes, contributing up to 30% of thyroid weight. Neural crest derived cells are contributed by the abortive fifth branchial pouch. These neural crest cells of the ultimobranchial body ultimately migrate into the upper third of the thyroid lobes giving rise to the parafollicular cells or calcitonin-secreting “C-cells.” In the developed thyroid, the point of fusion of this lateral thyroid anlage may be recognized as the “tubercle Zuckerkandl” located on the posterior surface of the thyroid lobe, an anatomical landmark useful in identifying the recurrent nerve (2). Recognizable thyroid follicles begin to appear around the second month, with most follicles having been formed by the fourth month. Iodine uptake occurs early and is present before mature follicles are identifiable.

The thyroglossal duct may completely disappear or remain intact, leaving an epithelial tube or cord—thus setting the stage for development of a thyroglossal duct cyst (3). These solitary cysts are generally smooth and well defined; most are midline and attached to the hyoid bone and can be seen to rise in the anterior neck when the tongue is protruded. Most cysts are recognized in childhood, but one third appear after the age of 30 years. A connection or potential connection to the foramen cecum predisposes to infection with oral flora. The resulting infection may cause spontaneous rupture with development of a thyroglossal sinus. The cysts are typically lined by either pseudostratified ciliated columnar epithelium, squamous epithelium, or both. In 20% of cases, the fibrous wall may contain heterotopic thyroid tissue in addition to chronic inflammatory infiltrate. It is said that approximately 1% of thyroglossal cysts will undergo malignant transformation, which is most commonly of the papillary variety, although squamous cell cancers are also seen.

A caudal midline thyroglossal remnant attached to the isthmus or adjacent thyroid lobe may become the pyramidal lobe. Present in about 50% of patients, the pyramidal lobe can extend cephalad, a variable distance toward the hyoid bone. Failure to recognize and remove this extension is a common cause of “incomplete total thyroidectomy.” Occasionally, the pyramidal lobe is attached to the hyoid bone by a fibrous band—the obliterated thyroglossal duct. When muscle fibers are identified in this band or cord, it has been dubbed the “levator glandulae superioris.”

Anomalous formation of the thyroid can lead to failure of descent and lingual thyroid or thyroid tissue in the submental area, hyoid bone region, or anywhere along the normal pathway of descent. Such abnormal positioning may be misinterpreted as a thyroglossal duct cyst. Thyrothymic thyroid rests, which are attached to the thyroid gland by connective tissue, are common. Occasionally, such nodules are recognized to descend into the anterior or posterior mediastinum, possibly giving rise to retrosternal goiters. Blood supply of these aberrant nodules usually arises from the inferior thyroid artery. In a recent study, Sackett et al studied 100 patients for thyrothymic rests, examining 180 sides of the neck in 90 individuals. Eighty-three separate sides (46%) revealed histologic thyroid rests. In those patients with recognized rests, 57% were bilateral, 30% right sided, and only 13% left sided. Eighty percent of rests were attached to the thyroid gland, 20% entirely separate, and 88% < 1 cm in size (4). It has been speculated that thyrothymic rests that remain after thyroidectomy may account for the occasional failure of total thyroidectomy. Clearly, this is a finding that has not been recognized by thyroid surgeons in the past.

Our understanding of the genetics of the thyroid development and control of embryologic migration is evolving. Mouse chromosome 4 is the location of Ttf-2, which is expressed in the developing thyroid. Gene expression is down-regulated, as thyroid cell precursors complete migration. Ttf-2 null mutant mice exhibit only sublingual thyroid or a total agenesis of the thyroid gland. Heterozygous mutations in Pax-8 are associated with hemiagenesis (5). Murine HoxA3 disruption results in thyroid hypoplasia. However, the exact molecular mechanisms of thyroid development remain to be elucidated.

Recurrent Laryngeal Nerve

Embryologic formation of the recurrent laryngeal nerves is intimately associated with the sixth branchial arch. The vagus nerve primordia is recognizable by the fifth week of fetal life, with the recurrent nerve clearly discernible by the sixth to seventh week (6). The embryonic aortic arches initially lie cranial to the larynx, so the recurrent nerve passes directly to the larynx. However, with further development the larynx moves cranially, the neck lengthens, while the aortic arch remains in the thorax. The recurrent nerve descending laterally must course medially under the sixth arch to maintain intimate contact with the larynx. Thus a medial “looping pathway” for the recurrent nerve is established. On the right side the sixth arch disappears and the fifth is transitory, so the nerve ascends to loop around the proximal portion of the fourth arch, which ultimately becomes the subclavian artery. The sixth arch on the left becomes the ductus arteriosus, so one finds the recurrent nerve on the left coursing under and around this structure (ligamentum arteriosum).

The blood supply of the recurrent laryngeal nerve arises from the inferior thyroid artery. The nerve enters the neck from behind the clavicle and the subclavian vessel on the right and the aorta on the left, coursing cephalad in the tracheoesophageal groove. Frequently, the right nerve ascends slightly lateral to the groove, while the left tends to course more medially in the groove. Approximately 50% of the time a nerve branches along its course into ventral and dorsal branches, with the dorsal branch innervating the esophagus and the ventral branch the larynx. Occasionally, more than two branches may be observed. The nerve is intimately associated with the inferior thyroid, crossing it at an oblique angle. It may cross dorsally or ventrally or between branches of the artery. This unpredictable anatomical situation is a constant source of concern to the thyroid surgeon because of the potential of inadvertent injury.

The surgeon must be aware of anatomical anomalies of the recurrent nerve that may be encountered. The most common is the “nonrecurring” recurrent nerve on the right side (~1%). This anomaly occurs as a result of the absence of the proximal portion of the fourth arch, with the right subclavian artery arising from the distal aortic arch and passing behind the esophagus. As a result, the right recurrent nerve courses directly from the vagus in the neck and enters the cricothyroid membrane behind the inferior cornu of thyroid cartilage from the area of the upper pole of the thyroid. The nerve can approach the thyroid gland in a course parallel with the inferior thyroid artery and can thus be confused as a vascular structure. A right aortic arch with the ligamentum arteriosum, which in two thirds of cases is associated with a left retro esophageal subclavian artery, will set the anatomical stage for a “nonrecurring” left recurrent nerve. This is an exceedingly rare occurrence. Preoperative imaging studies, especially CT, may alert the surgeon to these recurrent nerve anomalies.

The superior laryngeal nerve is a second nerve related to thyroid anatomy. It arises from the caudal end of the nodose ganglia after the vagus nerve exits the jugular foramen. It passes caudally deep to the carotid artery and along the pharynx toward the superior cornu of the thyroid cartilage, where it divides into a large internal branch (sensory to the epiglottis, base of the tongue, and larynx) and a smaller external branch (motor to the cricothyroideus and the inferior phargeal constrictors, with some sensory fibers to the intralaryngeal mucous membrane) (7). The external branch of the superior laryngeal nerve chiefly tenses the vocal cord, resulting in the timbre of the voice. As the nerve approaches the cricothyroid muscle, it is in close relationship to the superior thyroid artery and thus may be injured during thyroid surgery, requiring ligation of the upper pole vascular pedicle. At the operating table, it is affectionately known as the “nerve of Amelita Galli-Curci,” after the Italian coloratura soprano who lost the exquisite quality of her voice after goiter surgery (although speculated to have been the result of nerve injury) in 1930.

GROSS ANATOMY

The normal adult thyroid gland lies anterior to the upper trachea and consists of two lateral lobes connected by a midline isthmus. Each lobe is approximately 5 cm in length, 3 cm in width, and 2 cm in thickness. The superior pole of the lateral lobe is applied medially to the thyroid cartilage and cricothyroid muscle, posteriorly against the inferior pharyngeal constrictors and esophagus. Laterally, the lobe is adjacent to the carotid artery. The middle portion of the thyroid lobe is molded medially by the trachea, while laterally the gland abuts the carotid artery. The inferior pole lies laterally on the trachea at the level of the fourth and fifth tracheal ring. The average adult thyroid weighs between 20 and 30 g. The thyroid is covered by the sternohyoid muscle and most immediately by the sternothyroid muscle, which inserts into the thyroid cartilage in an oblique fashion and affectively prevents the lateral thyroid lobes from encroaching medially (Fig. 17.1).

FIGURE 17.1. Thyroid gland gross anatomy. (From Thorek P. Anatomy in surgery. Philadelphia: JB Lippincott Co, 1951:205, with permission.)

Blood Supply and Lymphatics

The arterial blood supply to the thyroid gland is derived from two main sources. The superior thyroid artery, first branch of the external carotid, descends parallel to the larynx to vascularize the upper pole. The inferior thyroid artery arises from the thyrocervical trunk and courses cephalad behind the carotid sheath to the level of the cricoid cartilage, turning medially and looping caudally to intersect the midportion of the thyroid gland. Near the capsule of the gland it divides into multiple terminal branches, one of which will generally supply the inferior parathyroid gland.

The thyroid gland is invested by the deep layer of cervical fascia, which forms a “filmy” capsule over the gland projecting into the thyroid substance, dividing the gland into irregularly shaped and sized lobules. Posteriorly, the fascia condenses forming the suspensory ligament of the thyroid (Berry's ligament), attaching the gland to the upper two or three tracheal rings. This dense attachment accounts for the up and down movement of the thyroid gland when the patient swallows. Additionally, the recurrent nerve often passes through Berry's ligament on its way to the cricothyroid membrane. The capsule provides a plane of surgical dissection between the gland, overlying sternohyoid, and sternothyroid muscles. Superficially, the thyroid surface is covered with multiple veins of varying size and a network of small lymphatic vessels. The veins for a plexus on the thyroid surface from which superior middle and inferior veins arise. The superior and middle vein empty into the jugular, while the inferior empties into the innominate vein.

The lymphatic drainage of the thyroid is profuse and flows in multiple directions. Intraglandular lymphatics communicate with capsular vessels, which may communicate diffusely across both lobes of the thyroid gland. The initial area of capsular drainage is felt to be the central or visceral compartment, defined as the space between the two common carotid arteries. Nodes in the visceral compartment may be divided into pretracheal, prelaryngeal, and paratracheoesophageal groups. Pretracheal nodes lie in anterior relationship to the isthmus and drain inferiorly into the mediastinal group, while the prelaryngeal nodes (delphian) drain cephalad toward the superior thyroid artery and into the lateral neck. Paratracheosophageal nodes lie deep to the thyroid lobe, running in relationship to the recurrent nerve, and ultimately communicate with lymph nodes lateral to the carotid artery. Central and lower thyroid pole lymphatics normally drain toward the paratracheosophageal nodes, while upper pole lymphatics follow the superior thyroid artery and thence to subdiagastric nodes in the lateral neck. Paratracheosophageal nodes also communicate with retroesophageal, tracheal, and retropharyngeal nodes (Fig. 17.2).

FIGURE 17.2. Lymphatic drainage of thyroid gland and central compartment. (From Weber CJ. In: Wood WC, Skandalkis JE. Anatomic basis of tumor surgery. St. Louis: Quality Medical Publishers, 1999:69, with permission.)

Central or visceral compartment nodes constitute primary lymphatic drainage, except for the upper thyroid poles, which drain to the lateral neck nodes. The lateral neck, internal jugular, supraclavicular, and posterior triangle nodes are areas of secondary drainage. Metastatic lateral nodes are managed by modified neck dissections with en bloc nodal excision, while preserving the jugular vein, the sternocleidomastoid muscle, and the accessory nerve.

PARATHYROID GLANDS

It is not possible to discuss the anatomy of the thyroid gland without mentioning the parathyroid glands. Usually there are four parathyroid glands, two located on each side of the trachea generally in close association with the thyroid gland. A small percentage of individuals who have five glands and an even smaller percentage will have only three. The superior parathyroid gland develops from the fourth branchial pouch along with the lateral lobes of the thyroid. These glands are generally found within a 1 cm radius of the inferior thyroid artery and are fairly constant. On the other hand, the inferior parathyroid glands arise from the third bronchial pouch along with the developing thymus and descend into the neck with the thymus tissue. Generally, they are found anterior to the recurrent nerve and in the area of the lower pole of the thyroid gland. They can be found under the capsule of the thyroid or intrathyroidal. In addition, their thymic association accounts for their occasional presence in the thymus in the lower neck or in the anterior mediastinum. Occasionally, the lower glands are found, along with thymic tissue, along the carotid sheath, in the path of descent into the neck of the parathymus.

Blood supply to both parathyroid glands is basically from the inferior thyroid artery, although in approximately 20% the superior parathyroid glands may be supplied by blood coming from the superior artery. There is symmetry between the superior parathyroid glands in approximately 80% of instances and 70% in the inferior glands (8).

REFERENCES

1. Halsted WS. The operative story of goiter. Johns Hopkins Medical Journal 1920;1:71–257.

2. Pelizzo MR, Toniato A, Gemo G. Zuckerkandl's tuberculum: an arrow pointing to the recurrent laryngeal nerve (constant anatomical landmark). J Am Coll Surg 1998;187:333–336.

3. Organ GM, Organ CH. Thyroid gland and surgery of the thyroglossal duct: exercise in applied embryology. World J Surg 2000; 24:886–890.

4. Sackett WR, Reeve TS, Barraclough B, et al. Thyrothymic thyroid rests: incidence and relationship to the thyroid gland. J Am Coll Surg 2002;195: 635–640.

5. Vliet GV. Developmental biology: frontiers for clinical genetics. Development of the thyroid gland: lessons from congenitally hypothyroid mice and men. Clin Genet 2003;63:445–455.

6. Gray SW, Skandalkis JE, Akin JT Jr. Embryological considerations of thyroid surgery: developmental anatomy of the thyroid, parathyroids and the recurrent laryngeal nerve. Am Surg 1976;42: 621–628.

7. Kierner AC, Aigner M, Burian M. The external branch of the superior laryngeal nerve, its topographical anatomy as related to surgery of the neck. Arch Otolaryngol Head Neck Surg 1998;124: 301–303.

8. Akerstrom G, Malmaeus J, Bergstrom R. Surgical anatomy of human parathyroid glands. Surgery 1984;95:14–21.