2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands

(1)

13 2.1 Embryology of the Thyroid

The primordial thyroid gland is first identifiable dur- ing the fourth week of gestation, beginning as an endodermal invagination of the tongue at the site of the foramen cecum (Fig. 2.1a). The foramen cecum lies where the midline intersects the sulcus termina- lis, which divides the tongue into anterior two thirds (oral part) and posterior one third (pharyngeal part).

The thyroid diverticulum begins its descent through the tongue carrying with it the thyroglossal duct. The path of descent carries the developing gland anterior to the hyoid bone and the larynx. During the descent in the fifth week, the superior part of the duct degen- erates. By this time, the gland has achieved its rudi- mentary shape with two lobes connected by an isth- mus. It continues to descend until it reaches the level of the cricoid cartilage at about the seventh week. By the twelfth week of development, thyroid hormone is secreted. The distal part of the thyroglossal duct de- generates but may remain as a pyramidal lobe [8].

There is also a contribution to the thyroid from the fifth pharyngeal pouch (ultimobranchial body).

These cells are believed to be neural crest in origin.

They migrate into the thyroid and differentiate into the calcitonin-producing C cells (Fig. 2.1a) [4].

A number of developmental errors can affect thy- roid development. The thyroid may fail to descend.

In this case, a lingual thyroid is located at the junc- tion of the oral and pharyngeal parts of the tongue (Fig. 2.1b). Ectopic thyroid tissue may occur at any point along the pathway of the descent of the thy- roid. In rare conditions, the thyroid may descend into the thorax. There may also be remnants of the thyroglossal duct that hypertrophy and become cys- tic (Fig. 2.1c). Ectopic thyroid tissue may also be en- countered laterally in the neck [9]. Evaluation of the patient should consider whether the ectopic tissue is the sole active thyroid tissue. In very rare circum- 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].

2.2 Embryology

of the Parathyroid Glands

The parathyroid glands develop from the third and fourth pharyngeal (branchial) pouches (Fig. 2.1a).

These pharyngeal pouches develop in association with the aortic arches that encircle the developing foregut. The pharyngeal arches have a mesodermal core, covered on their superficial surface by ectoderm and on their deep surface by endoderm. The pha- ryngeal pouches lie between successive pharyngeal arches and are endodermal evaginations of the fore- gut. The inferior parathyroid glands (parathyroid III) come from the third pharyngeal pouch and the supe- rior parathyroid glands (parathyroid IV) come from the fourth pharyngeal pouch. During the fifth week of development, the developing glands detach from the pouches and descend to join the thyroid gland during the seventh week. It should be noted that the inferior parathyroid glands actually arise from a more superior pharyngeal location (pouch III) than the su- perior thyroids (pouch IV). This relationship may be explained by the relationship of the developing infe- rior parathyroid gland with the thymus. The thymus arises from the caudal portion of the third pharyn- geal pouch. As the thymus descends into the thorax,

2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands

William B. Stewart and Lawrence J. Rizzolo

Contents

2.1 Embryology of the Thyroid . . . 13

2.2 Embryology of the Parathyroid Glands . . . 13 2.3 Anatomy of the Thyroid Gland . . . 14 2.3.1 General Topography and Relations . . . 14 2.3.2 Blood Supply . . . 15

2.4 Anatomy of the Parathyroid Glands . . . 17 2.5 Nearby Relations of the Thyroid and

Parathyroid at Risk During Surgery . . . 18 2.5.1 External Laryngeal Nerve . . . 18 2.5.2 Recurrent Laryngeal Nerve . . . 18

References . . . 19

(2)

William B. Stewart and Lawrence J. Rizzolo

14 it is accompanied by the inferior parathyroid glands.

Normally the attachment to the thymus is lost and the inferior parathyroid glands take up their normal posi-

tion posterior to the thyroid. Sometimes, however, the inferior parathyroid glands are carried into the thorax along with the thymus. The ectopic parathyroid gland may be found in a number of locations (Table 2.1).

The most common locations were intrathymic or par- aesophageal in the neck [13].

2.3 Anatomy of the Thyroid Gland

2.3.1 General Topography and Relations

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 from the medial portions of the left or right lobes. The thyroid extends from the level of the fifth cervical ver- tebra to the first thoracic vertebra. The gland weighs

Fig. 2.1 Embryology of the thyroid and parathyroid. a Schematic view from behind with the vertebral column, esophagus, and trachea 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 by Shen and co-workers [13]

Location Number

High cervical 1

Aorticopulmonary window 2

Posterior mediastinum 3

Carotid sheath 5

Intrathyroid 6

Anterior mediastinum (non-thymic) 9

Intrathymic 13

Paraesophageal (neck) 15

(3)

15

2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands

about 30 g, being somewhat heavier in females than in males [12]. The thyroid is surrounded by a sleeve of pretracheal fascia sometimes called the perithyroid sheath. Posteriorly, a thickening of this fascia attaches 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 the deep surface of the sternothyroid, sternohyoid, and omohyoid muscles (Figs. 2.2, 2.3). Where these muscles are absent in the midline, the isthmus of the gland is subcutaneous. Laterally the gland is related to the carotid sheath, which contains the common carotid artery, the internal jugular vein, and the va- gus nerve. Posteriorly, the superior parts of the lobes of the thyroid are related to the longus colli and lon- gus capitis muscles. Medially, the superior part of the thyroid is related to the larynx and laryngopharynx, which includes the cricothyroid and inferior pharyn- geal constrictor muscles and the thyroid and cricoid cartilages. Medially, the inferior part of the thyroid is related to the trachea and the esophagus. The isthmus

of the thyroid lies anterior to the second and third tracheal rings. The description of relationships to im- portant neural structures will be deferred to that sec- tion.

2.3.2 Blood Supply

As with other endocrine organs, the thyroid gland has a rich blood supply with abundant anastomoses. The arterial supply is bilateral from both the external ca- rotid system, through the superior thyroid artery, and the subclavian system, through the inferior thyroid branch of the thyrocervical trunk (Fig. 2.4). There may be a single thyroid ima artery that arises from the brachiocephalic artery.

The superior thyroid artery is normally the first branch of the external carotid artery, though fre- quently it may arise more inferiorly from the common carotid artery. This vessel descends to the superior pole of the thyroid along with the external laryngeal

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 arteries (red), veins (blue), and nerves (yellow). Note the close relationship of the superior pole of the thyroid gland with the carotid sheath and sympathetic chain

(4)

16 nerve. As it reaches the thyroid, the artery divides into anterior and posterior branches (Fig. 2.5). The anterior branch parallels the medial border of the lobe and anastomoses in the midline with the anterior branch of the other side. The posterior branch anasto- moses with branches of the inferior thyroid artery.

The inferior thyroid artery takes a looping course.

It ascends along the anterior scalene muscle (Fig. 2.3).

It turns medially to pass posteriorly to the carotid sheath and usually posteriorly to the sympathetic trunk as well. It descends along the longus colli to reach the inferior pole of the thyroid. There it passes to the thyroid either anteriorly or posteriorly to the recurrent laryngeal artery. At the thyroid, the artery branches into superior and inferior branches. The superior branch ascends on the posterior part of the

gland to anastomose with the posterior branch of the superior thyroid artery. The inferior branch supplies the inferior part of the gland as well as the inferior parathyroid glands. The inferior thyroid artery may be absent on either side. There is evidence that there are anthropologic differences in the incidence of thy- roid ima arteries, as well as in the symmetric origin of the superior thyroid arteries [17].

There are three main venous pathways from the thyroid: the superior, middle, and inferior thyroid veins (Fig. 2.6). The superior thyroid vein accompa- nies the superior thyroid artery and drains into the internal jugular vein. The middle thyroid vein is un- accompanied and drains directly into the internal jugular vein. Because of its posterior course, it is at risk when forward traction is applied to the gland, as

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 inferior thyroid artery follows a looping course. In this image it is seen superior to its origin from the thyrocervical trunk of the subclavian artery. 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

(5)

17 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. 2.7). The superior parathyroid glands normally lie at the level of the middle third of the thyroid, while the inferior parathyroid glands lie at the level of the inferior third. Generally, the superior parathyroid glands are supplied by the inferior thyroid artery, the

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

Fig. 2.5 Arterial supply of the thyroid derived from the four main vessels of the gland. Note the anterior and posterior divi- sions of the superior artery. The inferior thyroid artery comes from a posterolateral position to enter the thyroid gland close to the recurrent laryngeal nerve

Fig. 2.6 Venous drainage of the thyroid and parathyroid glands.

Superior, middle and inferior thyroid veins are indicated.

(6)

18 superior thyroid artery, or both. Anastomotic con- nections within the thyroid allow both vessels to con- tribute, especially to the superior parathyroid glands.

A number of methods have been advocated for local- izing the glands. These include ultrasonography [6], intraoperative methylene blue [7], and technetium sestamibi scans [18].

2.5 Nearby Relations

of the Thyroid and Parathyroid at Risk During Surgery

2.5.1 External Laryngeal Nerve

The external laryngeal is a division of the superior la- ryngeal nerve, a branch of the vagus. This nerve sup- plies the cricothyroid muscle. Since this muscle is in- volved in movements of the vocal apparatus, damage to the nerve will impair phonation. The nerve may run near the superior pole of the thyroid on the way

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- traction and division of the ligament to ensure that the nerve is preserved. There are some cases where the nerve may run through the substance of the gland [11,16].

In a small number of individuals (approximately 1%) the right subclavian artery arises distally from the arch of the aorta [1]. As a consequence the right recurrent laryngeal nerve is not pulled into the tho- rax by its relationship with the subclavian artery. This non-recurrent right laryngeal nerve passes directly to the larynx posterior to the common carotid artery.

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 surgery.

The vagus nerve and sympathetic trunk are within or closely related to the carotid sheath (Figs. 2.2, 2.3, 2.8). The vagus nerve may receive some of its blood supply from the inferior thyroid artery [15]. Conse- quently, the artery should not be ligated too close to its origin. Lymph node dissection along the carotid artery and near the vertebral artery or any manipu- lation near the superior pole of the thyroid gland should also be performed with care to ensure that the cervical sympathetic chain ganglia are not damaged or removed (Figs. 2.2, 2.3).

Fig. 2.7 Schematic dorsal view shows the course of the inferior laryngeal nerve in relation to the inferior thyroid artery, the thyroid gland, and the parathyroid glands

(7)

19 Removal of large thyroid tumors may require divi- sion of the infrahyoid muscles. Care must be taken to identify the branches of the ansa cervicalis that supply these muscles. The course of the ansa as it descends from the hypoglossal nerve is highly variable. Nor- mally, a superior division of the muscles will ensure the preservation of the nerve supply.

References

1. Abboud B, Aouad R (2004) Non-recurrent inferior laryngeal nerve in thyroid surgery: report of three cases and review of the literature. J Laryngol Otol 118:139–142 2. Bellantone R, Boscherini M, et al (2001) Is the identifica-

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

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 internal jugular vein

(8)

20

4. Dyson MD (1995) Endocrine system. In: Williams PL (ed) Gray’s anatomy. Churchill Livingstone, New York, pp 1881–1906

5. Ghanem N, Bley T, et al (2003) Ectopic thyroid gland in the porta hepatis and lingua. Thyroid 13:503–507 6. Haber RS, Kim CK, et al (2002) Ultrasonography for

preoperative localization of enlarged parathyroid glands in primary hyperparathyroidism: comparison with (99m)technetium sestamibi scintigraphy. Clin Endocrinol (Oxf) 57:241–249

7. Kuriloff DB, Sanborn KV (2004) Rapid intraoperative localization of parathyroid glands utilizing methylene blue infusion. Otolaryngol Head Neck Surg 131:616–622 8. Larsen WJ (2001) Human embryology. Churchill Living-

stone, New York

9. Livolsi VA (1990) Surgical pathology of the thyroid. Saun- ders, Philadelphia

10. Mirilas P, Skandalakis JE (2002) Benign anatomical mis- takes: the correct anatomical term for the recurrent laryngeal nerve. Am Surg 68:95–97

11. Page C, Foulon P, et al (2003) The inferior laryngeal nerve:

surgical and anatomic considerations. Report of 251 thy- roidectomies. Surg Radiol Anat 25:188–191

12. Shaheen OH (2003) Thyroid surgery. Parthenon Publish- ing, New York

13. Shen W, Duren M, et al (1996) Reoperation for persistent or recurrent primary hyperparathyroidism. Arch Surg 131:861–867; discussion 867–869

14. Sherman JH, Colborn GL (2003) Absence of the left inferior thyroid artery: clinical implications. Clin Anat 16:534–537

15. Skandalakis JE, Carlson GW, et al (2004) Neck. In: Skan- dalakis JE (ed) Surgical anatomy, vol 1. Paschalidis Medi- cal, Athens, pp 3–116

16. Sturniolo G, D’Alia C, et al (1999) The recurrent laryngeal nerve related to thyroid surgery. Am J Surg 177:485–488 17. Toni R, Della Casa C, et al (2003) Anthropological varia-

tions in the anatomy of the human thyroid arteries. Thy- roid 13:183–192

18. Udelsman R, Donovan PI (2004) Open minimally inva- sive parathyroid surgery. World J Surg 28:1224–1226