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Transcript
13
2
Embryology and Surgical Anatomy
of the Thyroid and Parathyroid Glands
William B. Stewart and Lawrence J. Rizzolo
Contents
2.1
2.2
2.3
2.3.1
2.3.2
2.4
2.5
2.5.1
2.5.2
2.1
Embryology of the Thyroid . . . 13
Embryology of the Parathyroid Glands . . . 13
Anatomy of the Thyroid Gland . . . 14
General Topography and Relations . . . 14
Blood Supply . . . 15
Anatomy of the Parathyroid Glands . . . 17
Nearby Relations of the Thyroid and
Parathyroid at Risk During Surgery . . . 18
External Laryngeal Nerve . . . 18
Recurrent Laryngeal Nerve . . . 18
References . . . 19
In this case, a lingual thyroid is located at the junction 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 thyroid. In rare conditions, the thyroid may descend
into the thorax. There may also be remnants of the
thyroglossal duct that hypertrophy and become cystic (Fig. 2.1c). Ectopic thyroid tissue may also be encountered laterally in the neck [9]. Evaluation of the
patient should consider whether the ectopic tissue
is the sole active thyroid tissue. In very rare circumstances 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].
Embryology of the Thyroid
The primordial thyroid gland is first identifiable during 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 terminalis, 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 degenerates. By this time, the gland has achieved its rudimentary shape with two lobes connected by an isthmus. 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 degenerates 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 thyroid development. The thyroid may fail to descend.
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 pharyngeal pouches lie between successive pharyngeal
arches and are endodermal evaginations of the foregut. The inferior parathyroid glands (parathyroid III)
come from the third pharyngeal pouch and the superior 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 superior thyroids (pouch IV). This relationship may be
explained by the relationship of the developing inferior parathyroid gland with the thymus. The thymus
arises from the caudal portion of the third pharyngeal 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, 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 Imaging, 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
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 paraesophageal 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 pyramidal 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 vertebra to the first thoracic vertebra. The gland weighs
2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands
Fig. 2.2 Thyroid gland and its relations at the level of the thyroid cartilage. An unembalmed cadaver was frozen and sectioned (Visible 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
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 lateral 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 vagus nerve. Posteriorly, the superior parts of the lobes
of the thyroid are related to the longus colli and longus capitis muscles. Medially, the superior part of the
thyroid is related to the larynx and laryngopharynx,
which includes the cricothyroid and inferior pharyngeal 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 important neural structures will be deferred to that section.
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 carotid 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 frequently 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
15
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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 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
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 anastomoses 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 thyroid 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 accompanies the superior thyroid artery and drains into the
internal jugular vein. The middle thyroid vein is unaccompanied 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
2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands
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. 2.6 Venous drainage of the thyroid and parathyroid glands.
Superior, middle and inferior thyroid veins are indicated.
in a thyroidectomy (Fig. 2.3). There are often a number of inferior thyroid veins that drain into the internal 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 arteries, lymphatic vessels may pass directly to the jugular
nodes. The medial aspect of the gland drains superiorly to the digastric nodes and inferiorly to the pretracheal and brachiocephalic nodes [15].
2.4
Fig. 2.5 Arterial supply of the thyroid derived from the four
main vessels of the gland. Note the anterior and posterior divisions of the superior artery. The inferior thyroid artery comes
from a posterolateral position to enter the thyroid gland close
to the recurrent laryngeal nerve
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
17
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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
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
superior thyroid artery, or both. Anastomotic connections within the thyroid allow both vessels to contribute, especially to the superior parathyroid glands.
A number of methods have been advocated for localizing 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 laryngeal nerve, a branch of the vagus. This nerve supplies the cricothyroid muscle. Since this muscle is involved 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
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 posteriorly 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 anteriorly 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 laryngeal 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 retraction 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 thorax 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]. Consequently, 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 manipulation 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).
2 Embryology and Surgical Anatomy of the Thyroid and Parathyroid Glands
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
Removal of large thyroid tumors may require division 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. Normally, a superior division of the muscles will ensure
the preservation of the nerve supply.
References
1.
2.
3.
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
Bellantone R, Boscherini M, et al (2001) Is the identification of the external branch of the superior laryngeal nerve
mandatory in thyroid operation? Results of a prospective
randomized study. Surgery 130:1055–1059
Droulias C, Tzinas S, et al (1976) The superior laryngeal
nerve. Am Surg 42:635–638
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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 Livingstone, New York
9. Livolsi VA (1990) Surgical pathology of the thyroid. Saunders, Philadelphia
10. Mirilas P, Skandalakis JE (2002) Benign anatomical mistakes: 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 thyroidectomies. Surg Radiol Anat 25:188–191
12. Shaheen OH (2003) Thyroid surgery. Parthenon Publishing, 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: Skandalakis JE (ed) Surgical anatomy, vol 1. Paschalidis Medical, 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 variations in the anatomy of the human thyroid arteries. Thyroid 13:183–192
18. Udelsman R, Donovan PI (2004) Open minimally invasive parathyroid surgery. World J Surg 28:1224–1226