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Home , Inferior thyroid artery, Inferior thyroid veins, Thyroglossal duct, Thyroid diverticulum

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2 and Surgical Anatomy of the and Parathyroid Glands

William B. Stewart and Lawrence J. Rizzolo

Contents In this case, a lingual thyroid is located at the junc- tion of the oral and pharyngeal parts of the 2.1 Embryology of the Thyroid . . 3. 1 (Fig. 2.1b). Ectopic thyroid tissue may occur at any 2.2 Embryology of the Parathyroid Glands . . . 13 point along the pathway of the descent of the thy- 2.3 Anatomy of the Thyroid Gland . . . 14 roid. In rare conditions, the thyroid may descend 2.3.1 General Topography and Relations . . . 14 into the thorax. There may also be remnants of the 2.3.2 Blood Supply . . . 15 that hypertrophy and become cys- 2.4 Anatomy of the Parathyroid Glands . . . 17 tic (Fig. 2.1c). Ectopic thyroid tissue may also be en- 2.5 Nearby Relations of the Thyroid and Parathyroid at Risk During Surgery . . . 18 countered laterally in the [9]. Evaluation of the 2.5.1 External Laryngeal Nerve . . . 18 patient should consider whether the ectopic tissue 2.5.2 Recurrent Laryngeal Nerve . . . 18 is the sole active thyroid tissue. In very rare circum- References . . . 19 stances thyroid tissue may be encountered inferior to the diaphragm in association with the gastrointestinal tract. This thyroid tissue, a struma ovarii, is derived from an ovarian germ cell tumor [5]. 2.1 Embryology of the Thyroid

The primordial thyroid gland is first identifiable dur- 2.2 Embryology ing the fourth week of gestation, beginning as an of the Parathyroid Glands endodermal invagination of the tongue at the site of the foramen cecum (Fig. 2.1a). The foramen cecum The parathyroid glands develop from the third and lies where the midline intersects the sulcus termina- fourth pharyngeal (branchial) pouches (Fig. 2.1a). lis, which divides the tongue into anterior two thirds These pharyngeal pouches develop in association (oral part) and posterior one third (pharyngeal part). with the aortic arches that encircle the developing The begins its descent through . The pharyngeal arches have a mesodermal the tongue carrying with it the thyroglossal duct. The core, covered on their superficial surface by ectoderm path of descent carries the developing gland anterior and on their deep surface by endoderm. The pha- to the and the . During the descent ryngeal pouches lie between successive pharyngeal in the fifth week, the superior part of the duct degen- arches and are endodermal evaginations of the fore- erates. By this time, the gland has achieved its rudi- gut. The inferior parathyroid glands (parathyroid III) mentary shape with two lobes connected by an isth- come from the third pharyngeal pouch and the supe- mus. It continues to descend until it reaches the level rior parathyroid glands (parathyroid IV) come from of the cricoid cartilage at about the seventh week. By the fourth pharyngeal pouch. During the fifth week the twelfth week of development, thyroid hormone is of development, the developing glands detach from secreted. The distal part of the thyroglossal duct de- the pouches and descend to join the thyroid gland generates but may remain as a pyramidal lobe [8]. during the seventh week. It should be noted that the There is also a contribution to the thyroid from inferior parathyroid glands actually arise from a more the fifth pharyngeal pouch (ultimobranchial body). superior pharyngeal location (pouch III) than the su- These cells are believed to be neural crest in origin. perior (pouch IV). This relationship may be They migrate into the thyroid and differentiate into explained by the relationship of the developing infe- the calcitonin-producing C cells (Fig. 2.1a) [4]. rior with the . The thymus A number of developmental errors can affect thy- arises from the caudal portion of the third pharyn- roid development. The thyroid may fail to descend. geal pouch. As the thymus descends into the thorax, 14 William B. Stewart and Lawrence J. Rizzolo

Fig. 2.1 Embryology of the thyroid and parathyroid. a Schematic view from behind with the vertebral column, , and removed. The foramen cecum and emerging thyroglossal duct are indicated in the tongue. Dashed arrow shows migration of thyroid along the anterior wall of the neck. Laterally, the pharyngeal pouches are numbered. These are evaginations of the foregut into the mesoderm that contains the aortic arches. Each pouch lies inferior to the aortic arch of the same number. The parathyroid glands originate in the pharyngeal pouches and migrate into position as indicated by the dashed arrows. Note the co-migration of the inferior parathyroids with the thymus gland. b CAT scan with intravenous contrast demonstrates the concentration of iodine into an undescended (lingual) thyroid gland. The anterior two thirds of the tongue lies anteriorly to the gland.c CAT scan at the level of the hyoid bone exhibits a thyroglossal duct cyst. b and c courtesy of Dr. James Abrahams, Department of Diagnostic Imag- ing, Yale University School of Medicine

Table 2.1 Location of 54 ectopic parathyroid glands identified tion posterior to the thyroid. Sometimes, however, the by Shen and co-workers [13] inferior parathyroid glands are carried into the thorax Location Number along with the thymus. The ectopic parathyroid gland may be found in a number of locations (Table 2.1). High cervical 1 The most common locations were intrathymic or par- Aorticopulmonary window 2 aesophageal in the neck [13]. Posterior mediastinum 3 5 Intrathyroid 6 2.3 Anatomy of the Thyroid Gland Anterior mediastinum (non-thymic) 9 2.3.1 General Topography and Relations Intrathymic 13 Paraesophageal (neck) 15 The right and left lobes of the thyroid are connected at the midline by the isthmus of the gland. A pyrami- dal lobe may extend superiorly from the isthmus or it is accompanied by the inferior parathyroid glands. from the medial portions of the left or right lobes. The Normally the attachment to the thymus is lost and the thyroid extends from the level of the fifth cervical ver- inferior parathyroid glands take up their normal posi- tebra to the first thoracic vertebra. The gland weighs 2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands 15

Fig. 2.2 Thyroid gland and its relations at the level of the thyroid cartilage. An unembalmed cadaver was frozen and sectioned (Vis- ible Human Project, National Institutes of Health). The orientation is the same as for a CAT scan with patient’s left on the right side of the image. Color enhancement demonstrates major (red), (blue), and nerves (yellow). Note the close relationship of the superior pole of the thyroid gland with the carotid sheath and sympathetic chain about 30 g, being somewhat heavier in females than of the thyroid lies anterior to the second and third in males [12]. The thyroid is surrounded by a sleeve tracheal rings. The description of relationships to im- of pretracheal fascia sometimes called the perithyroid portant neural structures will be deferred to that sec- sheath. Posteriorly, a thickening of this fascia attaches tion. the gland to the cricoid cartilage. This fascia is the lat- eral ligament of the thyroid (ligament of Berry). The anterior surface of the thyroid is related to 2.3.2 Blood Supply the deep surface of the sternothyroid, sternohyoid, and omohyoid muscles (Figs. 2.2, 2.3). Where these As with other endocrine organs, the thyroid gland has muscles are absent in the midline, the isthmus of the a rich blood supply with abundant anastomoses. The gland is subcutaneous. Laterally the gland is related arterial supply is bilateral from both the external ca- to the carotid sheath, which contains the common rotid system, through the superior thyroid , and carotid artery, the internal jugular , and the va- the subclavian system, through the inferior thyroid gus nerve. Posteriorly, the superior parts of the lobes branch of the (Fig. 2.4). There of the thyroid are related to the longus colli and lon- may be a single thyroid ima artery that arises from the gus capitis muscles. Medially, the superior part of the brachiocephalic artery. thyroid is related to the larynx and laryngopharynx, The is normally the first which includes the cricothyroid and inferior pharyn- branch of the , though fre- geal constrictor muscles and the thyroid and cricoid quently it may arise more inferiorly from the common cartilages. Medially, the inferior part of the thyroid is carotid artery. This vessel descends to the superior related to the trachea and the esophagus. The isthmus pole of the thyroid along with the external laryngeal 16 William B. Stewart and Lawrence J. Rizzolo

Fig. 2.3 Thyroid gland and its relations at the level of the third tracheal ring. Note the posteromedial relationships of the thyroid gland with the recurrent laryngeal nerve and middle thyroid veins. The thoracic duct green( ) is atypically dilated close to where it joins the left internal jugular and subclavian veins. The follows a looping course. In this image it iseen s su- perior to its origin from the thyrocervical trunk of the . It will loop superiorly and medially before descending to join the thyroid gland near the recurrent laryngeal nerve. An inferior right parathyroid gland (orange) is evident near the recurrent laryngeal nerve and middle thyroid veins. Major nerves (yellow), arteries (red), and veins (blue) are indicated

nerve. As it reaches the thyroid, the artery divides gland to anastomose with the posterior branch of the into anterior and posterior branches (Fig. 2.5). The superior thyroid artery. The inferior branch supplies anterior branch parallels the medial border of the the inferior part of the gland as well as the inferior lobe and anastomoses in the midline with the anterior parathyroid glands. The inferior thyroid artery may branch of the other side. The posterior branch anasto- be absent on either side. There is evidence that there moses with branches of the inferior thyroid artery. are anthropologic differences in the incidence of thy- The inferior thyroid artery takes a looping course. roid ima arteries, as well as in the symmetric origin of It ascends along the anterior scalene muscle (Fig. 2.3). the superior thyroid arteries [17]. It turns medially to pass posteriorly to the carotid There are three main venous pathways from the sheath and usually posteriorly to the sympathetic thyroid: the superior, middle, and inferior thyroid trunk as well. It descends along the longus colli to veins (Fig. 2.6). The superior thyroid vein accompa- reach the inferior pole of the thyroid. There it passes nies the superior thyroid artery and drains into the to the thyroid either anteriorly or posteriorly to the internal . The is un- recurrent laryngeal artery. At the thyroid, the artery accompanied and drains directly into the internal branches into superior and inferior branches. The jugular vein. Because of its posterior course, it is at superior branch ascends on the posterior part of the risk when forward traction is applied to the gland, as 2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands 17

Fig. 2.4 Arterial supply of thyroid and parathyroid glands is divided into a superior and a inferior system. Superior and in- ferior thyroid arteries are indicated.

Fig. 2.6 Venous drainage of the thyroid and parathyroid glands. Superior, middle and are indicated.

in a thyroidectomy (Fig. 2.3). There are often a num- ber of inferior thyroid veins that drain into the inter- nal jugular or the brachiocephalic veins. The lymphatic drainage of the lateral part of the thyroid follows the arterial supply. These lymphatic vessels either ascend with the superior thyroid artery or descend with the inferior thyroid artery to reach the jugular chain of nodes. Between these two arter- ies, lymphatic vessels may pass directly to the jugular nodes. The medial aspect of the gland drains superi- orly to the digastric nodes and inferiorly to the pre- tracheal and brachiocephalic nodes [15].

2.4 Anatomy of the Parathyroid Glands

There are normally two pairs of parathyroid glands, located along the posterior aspect of the thyroid gland Fig. 2.5 Arterial supply of the thyroid derived from the four (Fig. 2.7). The superior parathyroid glands normally main vessels of the gland. Note the anterior and posterior divi- lie at the level of the middle third of the thyroid, while sions of the superior artery. The inferior thyroid artery comes the inferior parathyroid glands lie at the level of the from a posterolateral position to enter the thyroid gland close inferior third. Generally, the superior parathyroid to the recurrent laryngeal nerve glands are supplied by the inferior thyroid artery, the 18 William B. Stewart and Lawrence J. Rizzolo

to its target. The external laryngeal nerve is frequently entrapped in the vascular pedicle that transmits the superior thyroid vessels. Consequently the nerve may be injured during the ligation of these vessels [2,3].

2.5.2 Recurrent Laryngeal Nerve

The recurrent laryngeal nerve, a branch of the vagus, supplies the remainder of the laryngeal musculature as well as sensation on and inferior to the vocal folds (Figs. 2.2, 2.3). On the right side, the nerve loops pos- teriorly to the subclavian artery to ascend obliquely until it reaches the tracheoesophageal groove near the inferior extent of the thyroid (Fig. 2.7). On the left side the nerve loops posteriorly to the arch of the aorta and ascends to the larynx in the tracheoesophageal groove. The nerve may divide into a number of branches that also supply the trachea and esophagus [10]. The nerve has a very close relationship with the inferior thyroid artery, where it might lie either an- teriorly or posteriorly to the vessel (Fig. 2.7). Because the left inferior thyroid artery may be absent in 6% of individuals, the identification of the recurrent la- ryngeal nerve may be more complicated [14]. The nerve may also be closely related to or within the ligament of Berry. Care must be taken in both re- Fig. 2.7 Schematic dorsal view shows the course of the inferior traction and division of the ligament to ensure that laryngeal nerve in relation to the inferior thyroid artery, the the nerve is preserved. There are some cases where thyroid gland, and the parathyroid glands the nerve may run through the substance of the gland [11,16]. In a small number of individuals (approximately superior thyroid artery, or both. Anastomotic con- 1%) the right subclavian artery arises distally from nections within the thyroid allow both vessels to con- the arch of the aorta [1]. As a consequence the right tribute, especially to the superior parathyroid glands. recurrent laryngeal nerve is not pulled into the tho- A number of methods have been advocated for local- rax by its relationship with the subclavian artery. This izing the glands. These include ultrasonography [6], non-recurrent right laryngeal nerve passes directly to intraoperative methylene blue [7], and technetium the larynx posterior to the . sestamibi scans [18]. It runs parallel to the inferior thyroid artery and can ascend for a short distance in the tracheoesophageal groove [15]. It is, therefore, at risk for injury during 2.5 Nearby Relations surgery. of the Thyroid and Parathyroid The vagus nerve and are within at Risk During Surgery or closely related to the carotid sheath (Figs. 2.2, 2.3, 2.8). The vagus nerve may receive some of its blood 2.5.1 External Laryngeal Nerve supply from the inferior thyroid artery [15]. Conse- quently, the artery should not be ligated too close to The external laryngeal is a division of the superior la- its origin. Lymph node dissection along the carotid ryngeal nerve, a branch of the vagus. This nerve sup- artery and near the or any manipu- plies the cricothyroid muscle. Since this muscle is in- lation near the superior pole of the thyroid gland volved in movements of the vocal apparatus, damage should also be performed with care to ensure that the to the nerve will impair phonation. The nerve may cervical sympathetic chain ganglia are not damaged run near the superior pole of the thyroid on the way or removed (Figs. 2.2, 2.3). 2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands 19

Fig. 2.8 Schematic anterior view depicts the courses of the superior and inferior laryngeal nerves in relation to the trachea and the larynx. Note also the course of the vagus nerve within the sheet of the common carotid artery and the

Removal of large thyroid tumors may require divi- References sion of the infrahyoid muscles. Care must be taken to identify the branches of the ansa cervicalis that supply 1. Abboud B, Aouad R (2004) Non-recurrent inferior laryn- these muscles. The course of the ansa as it descends geal nerve in thyroid surgery: report of three cases and from the hypoglossal nerve is highly variable. Nor- review of the literature. J Laryngol Otol 118:139–142 mally, a superior division of the muscles will ensure 2. Bellantone R, Boscherini M, et al (2001) Is the identifica- the preservation of the nerve supply. tion of the external branch of the superior laryngeal nerve mandatory in thyroid operation? Results of a prospective randomized study. Surgery 130:1055–1059 3. Droulias C, Tzinas S, et al (1976) The superior laryngeal nerve. Am Surg 42:635–638 20 William B. Stewart and Lawrence J. Rizzolo

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