Surgical Anatomy of the Thyroid and Parathyroid Glands

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The normal adult thyroid gland weighs about 17 g. It is wrapped around the anterolateral portion of the upper tracheal rings and larynx. Each lobe occupies a bed between the trachea and the esophagus medially; the carotid sheath posteriorly; and the sternocleidomastoid, the sternohyoid, and the sternothyroid muscles laterally and anteriorly. If the sternothyroid and sternohyoid muscles are to be divided transversely, they must be transected high, at the cricoid level, to preserve their motor nerve, the ansa hypoglossi. Section of the strap muscles has no clinical functional consequence.

The normal thyroid is soft, dark wine-red in color, and covered with a thin capsule. It is loosely attached to neighboring structures. The variations in fixation of the gland may arouse suspicion of pathologic change, particularly when the history suggests acute thyroiditis or cancer. Normally, the gland adheres only to the cricoid cartilage and the upper tracheal rings. This is the posterior suspensory, or Berry's, ligament.

The superior and inferior thyroid arteries are derived from the external carotid arteries and the thyrocervical trunks, respectively. Occasionally, a branch from the innominate artery or aorta, the arteria thyroidea ima, may be present. It passes directly upward in front of the trachea to enter the lower border of the isthmus. Its frequency of occurrence has been greatly overemphasized.

The superior thyroid artery is the first branch of the external carotid artery. It arises just above the thyroid cartilage. It gives off the superior laryngeal artery and then descends on the surface of the inferior constrictor of the pharynx, deep to the sternothyroid muscle. It enters the upper pole of the thyroid on its anterosuperior surface. It gives off a relatively

Nerve Run Superior Thyroid Artery
FIGURE 2-4. Relation between the external branch of the superior laryngeal nerve and the thyroid artery. The nerve may run partly to or around the artery or its branches.

large branch to the pyramidal lobe and isthmus. The superior thyroid artery, via its posterior branch, feeds the superior parathyroid or PIV. There is an extremely close relationship between the superior thyroid artery and the external branch of the superior laryngeal nerve (Fig. 2-4).20'21 This nerve is the motor nerve to the cricothyroid muscle, which produces tension of the vocal cord and makes possible the production of high-pitched voice sounds. Injuries to the nerve, in particular bilateral injuries, are easily overlooked at postoperative laryngoscopy. In 6% to 18% of cases, the external branch of the superior laryngeal nerve runs with or around the superior thyroid artery or its branches. Therefore, the nerve is highly vulnerable during ligation of the superior thyroid artery. Nevertheless, routine identification of the nerve during thyroid surgery is usually not advocated. Indeed, in 20% of cases, the nerve is not located in the surgically accessible area around the superior thyroid pole. It cannot be identified without dissection into or through the fibers of the pharyngeal constrictor muscle.

To avoid nerve injury when ligating the superior thyroid vascular pedicle, one may recommend first identifying the branches of the artery to avoid ligation of its main trunk. This identification is particularly recommended during excision of pathologically enlarged thyroid glands. The superior thyroid arteries should be ligated as low as possible on the thyroid gland. Second, it is advisable to dissect the superior thyroid vessels away from the nerve by opening up a space between the cricothyroid muscle and the upper pole of the thyroid. This dissection requires strong downward and outward traction on the upper pole of the gland. During this traction, the nerve should be sought more or less transversely between the superior thyroid vessels and the pharyngeal constrictor muscle or the cricothyroid muscle. Finally, the dissection must be performed from medial to lateral. Moreover, small vessels run from the superior thyroid artery into the pharyngeal constrictor and the cricothyroid muscles. As the nerve slips under these muscles, there is a risk of heat injury to the nerve during cauterization of these little muscular vascular branches.

The inferior thyroid artery arises from the thyrocervical trunk. It runs upward behind the carotid sheath to about the level of the cricoid cartilage, loops medially and downward to a level above the inferior pole of the thyroid, crossing the sympathetic trunk or its branches, and then runs upward again to reach the gland at its midportion. For the surgeon, the inferior thyroid artery appears from beneath the carotid artery only when the thyroid gland is retracted medially and the jugular vein laterally. This maneuver puts tension on the artery and makes it easier to identify. Before entering the thyroid, the artery usually divides into three branches: inferior, posterior, and internal. One branch or sometimes the trunk itself supplies the inferior parathyroid or P III.

The inferior thyroid artery and its terminal branches are intimately associated with the recurrent laryngeal nerve at about the level of the junctions of the lower and middle thirds of the thyroid gland (Fig. 2-5). The left recurrent laryngeal nerve ascends at the depth of the tracheoesophageal groove or just lateral to it at the lower pole of the thyroid. Usually it crosses deep to the inferior thyroid artery, sometimes between the terminal branches of the artery, rarely superficially. The right recurrent laryngeal nerve courses more obliquely, being somewhat more lateral in position caudally. It rarely crosses deep to the artery, usually between its terminal branches. Innumerable variations have been described.22 This is one of the most vulnerable areas for injury to the recurrent laryngeal nerve.

From a practical point of view, it is safer to search for the nerve below the artery. Identification of the inferior thyroid artery and careful ligation of its branches close to the gland is an excellent means of preserving the nerve and the inferior parathyroid. The recurrent nerve may be mistaken for one branch of the artery and especially for the inferior laryngeal artery. The nerve is somewhat less regular, rounded, and elastic than the artery. A small, red, sinuous vessel, a vasa nervorum, is always observed on it. The tortuousity of this small vessel is reduced when retraction of the thyroid puts the nerve under tension. Rarely, the nerve branches below the inferior thyroid artery. In any case, the surgeon must consider each extralaryngeal branch of the recurrent nerve as the possible motor branch and make every attempt to preserve them all.

Ligament Berry
FIGURE 2-5. Recurrent laryngeal nerve and its relationship to the inferior thyroid artery and to Berry's ligament. The nerve is embedded in the posterior portion of Berry's ligament. It is accompanied by the inferior laryngeal artery, which gives off a small branch that crosses the nerve internally.

The recurrent laryngeal nerve continues upward and medially at the posterolateral aspect of the middle third of the thyroid gland. It is extremely close to the capsule of the gland. In a few cases, particularly in pathologically enlarged glands, it may appear to penetrate or may actually penetrate the thyroid gland itself before entering the larynx. At the two upper tracheal rings, the nerve is embedded in the posterior portion of Berry's ligament (see Fig. 2-5). This ligament extends posteriorly behind the recurrent nerve and loosely attaches the thyroid to the esophagus. Vessels and connective tissue are more condensed anteriorly at the level of the tracheal rings. The nerve commonly divides before the point at which it enters the larynx, posterior to the cricothyroid muscle. The nerve is accompanied by the inferior laryngeal artery. At the site of Berry's ligament, this artery, usually just posterior to the recurrent nerve, gives off a small branch that crosses the nerve to enter the thyroid glands. Therefore, bleeding vessels in this portion of the ligament should never be clamped until the nerve has been identified. It is in this area that the recurrent nerve is most vulnerable to injury. Medial retraction on the thyroid lobe makes the nerve more vulnerable to injury during lobectomy. Indeed, this maneuver puts tension on the inferior thyroid artery and its branches and on Berry's ligament; consequently, the nerve is displaced anteriorly on the lateral aspect of the trachea. Moreover, the posterior fibers of Berry's ligament press the nerve against the lateral aspect of the tracheal rings, increasing the difficulties of dissection. Instead of medial retraction, it is preferable to retract the lobe upward after complete dissection of its lower pole. With this maneuver, it is easier to follow the nerve until its entry in the larynx at the level of the cricoid cartilage.

The recurrent laryngeal nerve is the motor nerve to the intrinsic muscles of the larynx.23 Injury to the motor trunk causes paralysis of the vocal cord on the ipsilateral side. The other extralaryngeal branches are sensory.

On rare occasions (0.63%), the right inferior laryngeal nerve does not recur.24 On the left side, this anomaly is quite exceptional (0.04%). As a rule, the origin of the nonrecurrent laryngeal nerve is cervical. Depending on its level of origin, the nerve runs more or less down along the vagus nerve and more or less across the jugulocarotid groove, making a downward curve. It always passes behind the common carotid artery. In one third of cases, it is in close contact with the trunk or the branches of the inferior thyroid artery; it enters the larynx at the usual level. Nonrecurrence of the inferior laryngeal nerve results from a vascular anomaly during embryonic development of the aortic arches: no innominate artery, but an aberrant subclavian artery (arteria lusoria). Nerve anomaly on the left side requires, in addition, a right aortic arch associated with situs inversus vis-cerum. A nonrecurrent laryngeal nerve has been also reported in association with an ipsilateral recurrent laryngeal nerve.25 28 Curiously, in some cases, no vascular anomaly has been demonstrated.26 The supposed coexistence of a recurrent and a nonrecurrent laryngeal nerve is questionable. First, an enlarged anastomotic branch between the cervical sympathetic system and the recurrent laryngeal nerve may be mistaken for nonrecurrent laryngeal nerve.29 Second, in the reported cases, it has never been demonstrated that the recurrent branch originated from the vagus nerve.

The nervous branch has only been described running in the usual pathway of a recurrent laryngeal nerve and having a small caliber. Whether this branch really originates from the vagus nerve and not from the sympathetic system, for example, the stellate ganglion, has not been proved.29

During thyroid lobectomy, if the nerve is not found at its usual place, before it crosses the inferior thyroid artery, it should be sought more or less transversely between the laterally retracted carotid sheath and the medially retracted thyroid in a plane that, in the case of nerve anomaly, cannot be cleaved as easily as usual, because the nonrecurrent inferior laryngeal nerve links the two structures.

Other aberrant pathways for the recurrent laryngeal nerve are observed only with pathologically enlarged thyroids and particularly with large posterior nodules and in substernal multinodular goiters. In these cases, if it is not possible to search for the nerve at its usual place, below the inferior thyroid artery, it should be located superiorly near to where it enters the larynx at the level of the cricoid cartilage. This maneuver requires previous dissection of the upper pole of the gland, or an "inside-out" approach, after section of the isthmus. Then the nerve should be dissected in a downward direction.

The venous drainage is more variable than the arterial supply. The capsular veins vary in size and may be enormous in pathologic glands. These are thin-walled structures that intercommunicate freely among themselves, forming a characteristic capsular network. The vessels within the gland itself are relatively small. Consequently, hemorrhage from capsular vessels may be important, but, provided that the vessels are clamped, subtotal resection of a lobe is a relatively bloodless procedure. The capsular network is schematically drained by three pedicles. The superior thyroid veins, just anterior and lateral to the superior thyroid artery, empty directly or indirectly into the internal jugular vein. The lateral or middle veins vary greatly in number. They pass directly from the anterolateral border of the lobe into the internal jugular vein. Careful lateral retraction of the carotid sheath facilitates their identification and their ligation, especially in enlarged glands where they may be mistaken for capsular veins. The inferior thyroid veins leave the lower pole and the isthmus in several trunks, frequently forming a plexus. They empty into the internal jugular vein and directly into the innominate vein. Ligation of the most lateral inferior thyroid veins requires previous identification of the recurrent nerve. The nerve may be anterior and, particularly when the thyroid lobe is medially retracted, could be mistaken for a vein. Follicular carcinomas, because of their high tendency for vascular invasion, may spread directly through veins into the internal jugular veins and sometimes downward into the innominate vein. In such cases, previous distal control of these veins is mandatory before thyroidectomy.

Lymphatic drainage of the thyroid is extensive and may flow practically in all directions. Capsular lymph channels, draining the intraglandular capillaries, may even cross-communicate with the isthmus and opposite lobe. Therefore, it is technically impossible to remove all the potential lymph node metastases in thyroid cancers.

Nevertheless, and from a practical point of view, the surgeon must consider two zones of lymphatic drainage for the

Thyroid Lymphatic Drainage
FIGURE 2-6. The two sites of lymphatic drainage of the thyroid. The first site is the visceral compartment of the neck. The second site is the lateral cervical region. The boundary between the two sites is the carotid sheath.

thyroid (Fig. 2-6). The first site is the paraglandular space or middle or visceral compartment of the neck. The second site is the lateral cervical region. The boundary between the two sites is the carotid sheath. In the visceral compartment, there are two groups: (1) the prelaryngeal and pretracheal and (2) the paratracheoesophageal. The prelaryngeal lymphatic vessels lie anterior to and above the isthmus and merge superiorly and laterally with the lymphatic vessels of the superior pole of the thyroid along the superior thyroid vessels to drain into the nodes of the lateral neck. The pretracheal lymphatic vessels lie below the isthmus and merge inferiorly with the lymphatic vessels of the anterior and superior mediastinum. The anterior boundary of the visceral compartment is the posterior surface of the prethyroid muscles, but sometimes node metastases may be found very anteriorly in the midline, particularly just above the isthmus (Delphian lymph nodes). The paratracheoesophageal lymphatic vessels lie along the lateral and posterior aspects of the thyroid gland and along the course of the recurrent laryngeal nerves. They communicate laterally with the lymphatic vessels in the supraclavicular triangles and posteriorly with those around and behind the trachea, the larynx, the pharynx, and the esophagus. Lymphatic drainage of the isthmus flows down into the mediastinal nodes and upward into the paralaryn-geal nodes. The normal flow direction from the central and lower parts of the lateral lobes is toward the tracheoesophageal nodes. Only lymphatic drainage of the superior poles of the lobes may flow directly into the lateral neck nodes. This may explain why papillary thyroid carcinomas revealed by metastatic laterocervical lymph nodes are located in the upper pole of thyroid lobes in nearly two thirds of cases.30 Therefore, the central neck area is the primary zone of lymphatic drainage for all thyroid cancers except those located in upper poles of the glands. Lateral neck areas (internal jugular chains and posterior triangles) are secondary zones of lymphatic drainage. Some of the involvement probably is brought about by retrograde extension resulting from obstruction of the lymph flow route in the central neck area.31

Because the visceral or central compartment of the neck is the primary zone of involvement, many surgeons advocate prophylactic neck dissection in this area in cases of papillary and medullary thyroid carcinomas. Indeed, even if metastatic nodal recurrences are rare, reoperations in the central neck area are difficult and increase the risk of injury to the recurrent laryngeal nerve and parathyroid glands.

lust as embryology helps the surgeon understand where the parathyroid glands are positioned, their gross appearance makes it possible to identify them and to differentiate them from other structures. The parathyroid glands vary in shape but remain compact in 94% to 98% of cases.5 Their color depends on their adipocyte content and vascularization: light brown or coffee colored when the gland is very fatty, and darker, buff, or reddish brown when the gland is more cellular or has a richer blood supply. They are soft and supple and retain their original shape during dissection. If flattened by the development of a thyroid nodule, they can become rounded again when detached from its surface. Their average size varies from 5.25 x 3 x 1.28 mm to 5 x 3 x 1 mm, as reported by Gilmour and Martin32 and Wang,6 respectively. The average weight of a normal gland is 40 mg (range, 10 to 78 mg). They are encapsulated and have sharp outlines and a smooth, glistening surface. Parathyroid glands have a particular affinity for fat and are often found completely or partially embedded in a fatty globule. They often have a fatty capsule over their surface like the crest of a helmet. Characteristically, they can be separated easily from the adjacent fatty structures.

Whatever their size, shape, or color, the parathyroid glands always share an encapsulated appearance, which gives them a proper shape, an ocher tint, and a soft elastic consistency. Fat is softer, paler, and straw colored, with no definite shape. Thyroid tissue is firmer, less homogeneous, darker wine-red in color with bluish-gray tints, and often embedded in "padding." Lymph nodes are firmer, more rounded, less homogeneous, and white, dirty gray, or putty colored, with black dots. Nodes are separated from the adjacent fat with greater difficulty. Lymph nodes are usually multiple. Thymic tissue is paler, grayish yellow or grayish pink, granular, and adherent to the fat.

The arterial supply of the parathyroid glands is terminal in type; the artery is solitary in two thirds of cases. The length of the artery varies (1 to 40 mm), but in cases of thyroidectomy, even if the parathyroid is pedicled, its preservation depends primarily on the distance between the origin of its artery and the thyroid capsule. The vascularization of P III depends primarily on the inferior thyroid artery. The P IV are supplied by the inferior thyroid artery, by the posterior branch of the superior thyroid artery, or by the posterior marginal arch of Evans. Both P III and PIV may be entirely dependent on the inferior thyroid artery. Therefore, during thyroid lobectomy, the inferior thyroid artery must never be ligated at the level of its main trunk. Similarly, the preservation of P IV requires separate ligation of the branches of the superior thyroid artery so as to preserve the posterior branch. At the lower poles of the thyroid lobes, the preservation of P III is ensured by the technique of ultraligation advised by Halsted and Evans.33 When the lower parathyroid glands (P III) are situated in the thyrothymic ligaments or in the upper poles of the thymus, they are supplied by the inferior thyroid artery.

Venous drainage occurs by three methods: (1) by the capsular network of the thyroid, (2) by the venous pedicles of the thyroid body, or (3) by a combination. Thyroid lobectomy may render the ipsilateral parathyroid glands ischemic. Hemostasis of a parathyroid vein generally should be avoided because of the risk of glandular infarction. Parathyroid ischemia is often evidenced by progressive darkening of the gland. Incision of the capsule and superficial parenchyma may prevent venous stasis and allow the gland to recover its normal color.

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