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Clinical Anatomy 25:19–31 (2012)
REVIEW
Anatomy of Thyroid and Parathyroid Glands
and Neurovascular Relations
A. MOHEBATI
AND
A.R. SHAHA*
Head and Neck Service, Memorial Sloan Kettering Cancer Center, New York, New York
Historically, thyroid surgery has been fraught with complications. Injury to the
recurrent laryngeal nerve, superior laryngeal nerve, or the parathyroid glands
may result in profound life-long consequences for the patient. To minimize the
morbidity of the operation, a surgeon must have an in-depth understanding of
the anatomy of the thyroid and parathyroid glands and be able to apply this
information to perform a safe and effective operation. This article will review
the pertinent anatomy and embryology of the thyroid and parathyroid glands
and the critical structures that lie in their proximity. This information should
aid the surgeon in appropriate identification and preservation of the function
of these structures and to avoid the pitfalls of the operation. Clin. Anat.
25:19–31, 2012. V 2011 Wiley Periodicals, Inc.
C
Key words: thyroid; parathyroid; anatomy; recurrent laryngeal nerve; superior
laryngeal nerve; embryology
INTRODUCTION
EMBRYOLOGY OF THYROID GLAND
In-depth knowledge of the anatomical relations
and variations of the thyroid and parathyroid
glands, vascular supply, and laryngeal nerves is
the cornerstone for performing safe thyroid or
parathyroid surgeries. Early thyroidectomies were
fraught with major complications with mortality
rate as high as 40% during the first half of the
19th century (Hegner, 1932; Hanbury and Boyd,
1963). During this period, thyroidectomy was
advised to be performed only in emergency situations. Many surgeons, including Billroth, Kocher,
and Halsted extensively studied the vascular anatomy of thyroid and modified their surgical technique in an attempt to decrease the morbidity and
the mortality of this operation. As the understanding of the anatomy of the thyroid, parathyroid
glands, the laryngeal nerves and vascular anatomy
improved over the second half of the 19th century
and with the improvement of surgical instruments,
this operation became safer. In 1917, Theodore
Kocher reported his mortality rate from thyroid surgery as less than 0.2% before the Swiss Surgical
Congress (Hegner, 1932). To date, the thorough
understanding of the thyroid and parathyroid
glands anatomy and embryology has been most
important in improving the safety and efficacy of
thyroid surgery.
The development of thyroid gland begins by the
third week of gestation and ends by the eleventh
week. The primordium of the medial part of the thyroid gland appears during the third week of gestation
as an epithelial proliferation in the floor of the pharynx immediately caudal to the tuberculum impar at
the border of the first and second pharyngeal
pouches (Sadler and Langman, 2006). It appears as
a duct like invagination of the endoderm in the floor
of the pharynx. This point of origin of the thyroid
gland is later called the foramen cecum. This midline
structure undergoes successive changes such as
enlargement, bifurcation, lobulation, and detachment from the pharynx. Subsequently, the thyroid
descends from the floor of the pharynx in front of
the hyoid bone and the lingual cartilage to its final
position anterior to the trachea by the end of the
C 2011
V
Wiley Periodicals, Inc.
*Correspondence to: Ashok R. Shaha, Jatin P. Shah Chair in Head
and Neck Surgery and Oncology, Memorial Sloan Kettering Cancer
Center, Head and Neck Service, 444 E 68th Street, Mailbox 294,
New York, NY 10065, USA. E-mail: [email protected]
Received 13 January 2011; Revised 7 May 2011; Accepted 23
May 2011
Published online 28 July 2011 in Wiley
(wileyonlinelibrary.com). DOI 10.1002/ca.21220
Online
Library
20
Mohebati and Shaha
seventh week of gestation (Hoyes and Kershaw,
1985). The lateral thyroid primordia originate from
the fourth and fifth pharyngeal pouches, descend to
join the medial primordium by the fifth week of gestation contributing to up to 30% of the weight of the
gland (Organ and Organ, 2000). The lateral thyroid
anlage arises from the neural crest cells and provide
the parafollicular C cells that produce calcitonin
(Sugiyama, 1971). By the seventh week, the gland
consists of a median isthmus and two lateral lobes
(Sadler and Langman, 2006). During this migration,
the thyroid remains connected to the tongue by the
thyroglossal duct which later obliterates and may be
represented by a strip of fibrous or muscular tissue.
The lingual part of the thyroglossal duct may remain
identifiable until late in the fetal life (Hoyes and
Kershaw, 1985). A thyroglossal cyst may be present
at any point along the migratory path of the thyroid
gland near the midline of the neck due to incomplete
degeneration of the duct. Thyroid follicles begin to
appear by the second month and most are formed by
the end of the fourth month of gestation. After this
period, additional growth is achieved by enlargement
of the follicles (Gray et al., 1976). By approximately
the end of the third month, follicles containing colloid
become visible (Sadler and Langman, 2006). The
embryonic thyroid begins to incorporate iodine and
produce and secrete thyroid hormone into the circulatory system as early as the 10th to 12th week of
gestation (Larsen et al., 2001).
In order to fully understand the various pathologies
that may arise from the thyroid tissue, understanding
the development of its surrounding structures is
essential. One should bear in mind that ectopic thymic tissue may be found near or within the thyroid
gland (Chan and Rosai, 1991; Ito et al., 2007). Thymus shares its origin with the inferior parathyroid
glands. It originates from the ventral portion of the
third pharyngeal pouch and descends down toward
the mediastinum. Ectopic or accessory thymic tissue
may be found anywhere along this tract near or even
within the thyroid gland. The level of the thyroid
gland is the most common site of the ectopic thymic
tissue (Wu et al., 2001).
ECTOPIC THYROID GLAND
In the course of the development of thyroid, part of
the gland or the whole gland may fail to reach its final
position. In some patients accessory ectopic thyroid
tissue may be found in the presence of thyroid gland in
its normal anatomic position. This tissue may be functional; however, it is usually inadequate to maintain
the normal function of the thyroid if the main gland is
removed. Ectopic thyroid tissue has been reported in
oropharynx, infrathryoid region, mediastinum, larynx,
trachea, and esophagus (Strickland et al., 1969;
Myers and Pantangco, 1975; Kamat et al., 1979;
Noyek and Friedberg, 1981; Arriaga and Myers, 1988;
Ferlito et al., 1988; Rubenfeld et al., 1988; BowenWright and Jonklaas, 2005). Lingual thyroid, although
rare, is the most common site of ectopic thyroid tissue
with reported frequency of 1/3,000 to 1/10,000 individuals (Noyek and Friedberg, 1981; Williams et al.,
1996). The first case was reported by Hickman in
1869 that showed a large lingual thyroid gland without the presence of the gland in its normal location
(Weider and Parker, 1977). There is a higher incidence of ectopic lingual thyroid tissue in females
with the female to male ratio of 3:1–7:1 (Neinas
et al., 1973; Noyek and Friedberg, 1981; Williams
et al., 1996; Massine et al., 2001). It is the only thyroid tissue in 70–100% of the affected individuals,
and hypothyroidism at the time of diagnosis is the
more common presenting symptom in these patients
(Massine et al., 2001; Yoon et al., 2007).
Lingual thyroid is an embryonic malformation that
typically occupies a median position at the base of
the tongue between the foramen cecum and the epiglottis. It often presents as a rounded lobulated
mass covered with normal mucosa with varying
degree of vascularity and a different hue from the
surrounding tongue tissue (Waters et al., 1953). In a
study by Sauk to identify the incidence of ectopic lingual thyroid tissue, 200 cadaveric dissections were
performed. In this study ectopic lingual thyroid tissue was identified at a higher incidence of 10% of
the individuals affecting both sexes equally. Seventy-five percent of the ectopic thyroid tissue was
located at the foramen cecum, and the remaining
25% was located rostrally along a 6-cm segment.
The histologic pattern was consistent with mature
thyroid tissue only in 25% of all cases (Sauk, 1970).
THYROID GLAND SHAPE AND SIZE
The Germans call the thyroid gland Scilddrüse or
the ‘‘shield gland,’’ but the English word for the thyroid gland is derived from the Greek word thyreoeidos
(Thyreos – sheild, eidos – from) with the same meaning. It consists of two lateral lobes which are united
by isthmus located anterior to the trachea and weighs
about 15–25 g in adults (Hoyes and Kershaw, 1985).
The thyroid lobes measure about 4 cm superiorly to
inferiorly, 15–20 mm in width and the thickness of
20–39 mm (DeGroot et al., 1996). One should keep
in mind that these dimensions may be drastically
altered due to disease. The gland is covered by a thin
fibrous capsule without true lobulations. The lateral
lobes of the thyroid are located between the trachea
and larynx medially and the carotid sheath and sternocleidomastoid muscle laterally. Laterally, the deep
cervical fascia creates a loose false capsule on lateral
portion of the gland (DeGroot et al., 1996). Anteriorly, the gland is covered by the superficial fascia and
plathysma, and, posteriorly, the condensation of the
deep cervical fascia forms the suspensory ligament of
Berry affixing the thyroid to the trachea and larynx
(Hoyes and Kershaw, 1985; Sasou et al., 1998). The
ligament is attached to the inferior margin of the
cornu of the cricoid cartilage extending inferio-medially onto the tracheal wall attaching the thyroid to the
first two tracheal rings (Leow and Webb, 1998). The
ligament’s tethering of the thyroid to the trachea is
responsible for elevation of the thyroid during deglutition (Fig. 1). The external thyroid capsule is shown to
be deficient in the anterior midline. It has been
reported that Levator glandulae thyroideae (LGT)
Thyroid and Parathyroid Glands and Neurovascular Relations
21
Fig. 1. Posterior and lateral views of the recurrent laryngeal nerves in the chest
and neck as they course in the tracheoesophageal groove and innervate the larynx.
Reprinted with permission from Randolph (2003), p. 305.
fibers often present intermixed with follicular elements in this region (Mete et al., 2010). LGT is
described as an occasional paired or unpaired muscle
that extends from the hyoid bone to the isthmus of
the pyramidal lobe more frequently on the left side
(Hollinshead, 1968; Loukas et al., 2008). The
reported incidence of LGT varies from 0.49% to 58%
(Lehr, 1979; Harjeet et al., 2004; Ranade et al.,
2008). This is particularly important and may become
a potential pitfall in pathologic staging of thyroid cancer. An enlargement of the lateral edge of the thyroid
lobe that stems from the fusion of the lateral and
medial thyroid anlages is called the tubercle of Zukerkandl. It is an anatomical landmark that may be used
in identifying the RLN, and it is closely associated with
the superior parathyroid glands. The RLN generally
courses deep to this structure and superficial to the
lateral border of the trachea. However, this relationship can vary due to the enlargement of the tuberculum placing the RLN at risk of injury during exploration (Fig. 2). A detailed relationship of the recurrent
laryngeal nerve, vascular supply, and the parathyroid
glands to the thyroid will be discussed.
sal duct and may be attached to the hyoid bone by a
band of fibrous tissue (Mansberger and Wei, 1993).
In a study of 60 cadavers, the pyramidal lobe was
present in 55% of the cadavers and branched off
more frequently from the left part of the isthmus
(Braun et al., 2007). Its median length in men was
14 and 29 mm in women. Marshall, in his review of
the anatomic variations of the thyroid gland in 60
cases, reported the presence of pyramidal lobe in
43% of the subjects (Marshall, 1895). The incidence
of pyramidal lobe is reported between 15% and 75%
in the literature (Marshall, 1895; Levy et al., 1982;
Savage et al., 1984; Braun et al., 2007; Sturniolo
et al., 2008). The isthmus unites the two lateral lobes
of the thyroid gland. It is reported to be about 20 mm
in length and width and about 2–6 mm in thickness
and located anterior to the second and third tracheal
rings (Hoyes and Kershaw, 1985). In his report, Marshall noted that in 7% of the cases, one lobe was
grossly larger than the other lobe and the isthmus
was absent in 10% of the cases (Marshall, 1895). In
another series of 58 cases, the isthmus was absent in
6.9% of the subjects (Braun et al., 2007).
PYRAMIDAL LOBE AND ISTHMUS
EMBRYOLOGY OF PARATHYROID
GLANDS
The pyramidal lobe is a potential pitfall of thyroid
surgery and could be a source of recurrent disease if
it is left behind during thyroid surgery. The pyramidal
lobe represents the inferior portion of the thyroglos-
The parathyroid glands are endodermal in origin
and develop from the dorsal wing of the third and
fourth pharyngeal pouches (Larsen et al., 2001;
22
Mohebati and Shaha
Fig. 2. Variation in anatomic relationships of the
recurrent laryngeal nerve and the tuberculum Zuckerkandl. The RLN usually courses superficial to the lateral
border of the trachea and deep to the tuberculum (A).
However, it may run medial (B) or be displaced laterally
(C) due to nodular enlargement of the thyroid tissue. This
variation if unrecognized will place the RLN at risk of
injury. IC, inferior constrictor muscle; CP, cricopharyngeus muscle; CT, cricothyroid muscle. (Courtesy of the Memorial Sloan-Kettering Cancer Center, New York, NY;
with permission.) [Color figure can be viewed in the
online issue, which is available at wileyonlinelibrary.com.]
Fig. 3. Variable relationship of the recurrent laryngeal nerve and the branches of
inferior thyroid artery. It more commonly courses deep to ITA (A), but can also travel
anterior (B) to or in between (C) the branches of ITA. (Courtesy of the Memorial
Sloan-Kettering Cancer Center, New York, NY; with permission.) [Color figure can be
viewed in the online issue, which is available at wileyonlinelibrary.com.]
Thyroid and Parathyroid Glands and Neurovascular Relations
Sadler and Langman, 2006). The first detailed anatomic description of the parathyroid glands was published by Welsh in 1898 and subsequently by Halsted
and Evans in 1907, making a distinction between the
superior and the inferior glands (Welsh, 1898;
Halsted and Evans, 1907). Their function is to produce parathyroid hormone (PTH) which regulates the
circulating level of calcium through intestinal and renal absorption and bone remodeling. There are typically four parathyroid glands; however, supernumerary glands and less than four glands have been
reported. In a reported series of 428 cases, 0.5%
had six glands, 25% had five glands, 87% had four
glands, and 6.1% of the cases had three glands
(Alveryd, 1968). In another series, more than four
glands were found in 13% of the cases, four
glands in 84%, and three glands in 3% of the cases
(Akerstrom et al., 1984). The majority of the supernumerary glands were either rudimentary or divided
weighing as little as less than 5 mg and in close proximity of a normal gland. The combined weight of the
normal parathyroid glands reported from 106 to 166
mg in men and 130–168 mg in women with each
gland weighing about 30–40 mg (Alveryd, 1968;
Fancy et al., 2010). The color of each gland varies
from yellow to reddish brown, measuring about 3–
8 mm and are usually oval shaped (Fancy et al.,
2010). The inferior thyroid artery is the predominant
vascular supply to both upper and lower parathyroid
glands in 76–86% of the cases (Alveryd, 1968).
The superior parathyroid glands originate from the
fourth pharyngeal pouch, and as they lose their
attachment with the pharyngeal wall, they attach to
the posterior surface of the caudally migrating thyroid (Sadler and Langman, 2006; Fancy et al.,
2010). They have a much shorter migration distance
compared to the inferior parathyroid glands accounting for their more predictable location. They are
generally at the level of the upper two-thirds of the
thyroid. In an autopsy study of 503 cases, 80% of
the superior glands were located on the posterior aspect of the thyroid gland within a circumscribed area
2cm in diameter about 1 cm above the crossing point
of the recurrent laryngeal nerve and inferior thyroid
artery (Akerstrom et al., 1984). In this study, the
ectopic superior parathyroid glands were found at
the level of the upper pole of the thyroid gland in 2%
of the subjects and above the pole on only 0.8% of
the subjects. Other ectopic positions of the superior
parathyroid glands such as in the posterior neck, retropharyngeal or retroesophageal space, and intrathyroidal position are quite rare and reported in up
to 1% of the cases (Wang, 1976; Akerstrom et al.,
1984).
While the dorsal wing of the third pharyngeal
pouch give rise to the inferior parathyroid glands,
the ventral wing gives rise to the thymus during the
fifth week of gestation (Sadler and Langman,
2006). As both primitive glands lose their connection with the pharyngeal wall, they join the thymus
as it travels caudally and medially to its final position in the mediastinum (Mansberger and Wei,
1993; Sadler and Langman, 2006). This migration
of the inferior parathyroid glands with the thymus
23
accounts for the fact that they are usually found in
a plane ventral to that of the superior parathyroid
glands (Mansberger and Wei, 1993). For the same
reason, ectopic inferior parathyroid glands can be
found anywhere along this large area of descent up
to the superior border of the pericardium (Gray
et al., 1976). In a study of 645 parathyroid glands
from 160 postmortem subjects, the inferior glands
were evenly distributed between the lower pole of
the thyroid and isthmus (Wang, 1976). In this
study, 42% of the inferior parathyroid glands were
found on the anterior or the postero-lateral surface
of the lower pole of the thyroid while 39% were
located in the lower neck in proximity to the thymic
tissue, 15% lateral to the thyroid, and only 2%
within the mediastinal thymic tissue. The persistence of the primitive attachment of the inferior
parathyroid glands to the thymus, during the thymic descent, may result in a more caudal placement
of the parathyroid glands. In this situation, the inferior parathyroid glands may be found at the level of
the anterior superior mediastinum in close proximity to the upper pole of thymic remnants (Kurtay
and Crile, 1969). Exploration of the superior mediastinum becomes important during four gland exploration when the inferior parathyroid glands cannot be identified in the neck.
A rare ectopic location that could be a source of
pitfall during parathyroid for surgery for hyperparathyroidism is the intrathyroid location of the parathyroid glands. Although the embryologic origin of this
ectopic location has been controversial, they can
originate from either the superior or the inferior
glands (Wang, 1981; Akerstrom et al., 1984; Kaplan
et al., 1992; Bahar et al., 2006). The incidence of
intrathyroid parathyroid gland is reported between
0.7% and 3.6% in the literature (Proye et al., 1994;
Bahar et al., 2006; Goodman et al., 2011). Additionally, because of their rarity, the intrathyroid parathyroid glands can be missed by preoperative imaging,
and this must be kept in mind when meticulous bilateral neck exploration fails to identify the hyperfunctioning gland.
In majority of the cases, parathyroid glands are
located in symmetrical position in the neck. Akerstr[dacute]om et al. in their study emphasized the close
proximity of the superior and the inferior parathyroid
glands and the thyroid. They found symmetrical
position of the superior and inferior glands in 80%
and 70% of the cases, respectively, with a relative
symmetry of 60% for all four glands (Akerstrom
et al., 1984).
VASCULAR ANATOMY
The thyroid gland derives its blood supply primarily from the superior and inferior thyroid arteries that
are generally constant. A third vessel, thyroidea ima
artery, in some cases may replace the inferior thyroid artery and become one of the principle arteries
supplying the gland. The venous drainage of the thyroid gland that is paralleled by the lymphatic drainage is supported by the superior, middle, and the inferior thyroid veins.
24
Mohebati and Shaha
ARTERIAL SUPPLY
The superior thyroid artery is most commonly
described as the first branch of the external carotid
artery arising close to the carotid bifurcation. It travels on the external surface of the inferior constrictor
muscles of the larynx, along with the superior thyroid
vein, entering the gland postero-medially just below
the highest point of the upper lobe (Mansberger and
Wei, 1993). At this point, it lies superficial to the
external branch of the superior laryngeal nerve
(Fancy et al., 2010). Just prior to entering the gland,
the superior thyroid artery may trifurcate with its
branches communicating with the interior thyroid artery and the contralateral thyroid lobe blood supply
through the isthmus (Mansberger and Wei, 1993).
The major three branches of the superior thyroid artery are the sternocleidomastoid branch, the ventral
medial, and the dorsal lateral branches. The ventral
medial branch is larger and communicates through
the isthmus with the branches from the contralateral
gland, while the dorsal lateral branch communicates
with the branches from the inferior thyroid artery on
the same side (Rossi et al., 1971). Although the common carotid artery usually has no branches, on occasion, the superior thyroid artery may arise from the
common carotid artery proximal to the bifurcation
(Smith and Benton, 1978; Akyol et al., 1997). The
reported incidence of origin of superior thyroid artery
from the common carotid in the literature varies from
5% to 45% and in majority of the cases within 1 cm
of the bifurcation (Smith and Benton, 1978). In one
series, the origin of the superior thyroid artery from
the common carotid was more common on the left
side than on the right (Vazquez et al., 2009).
The inferior thyroid artery is a branch of the thyrocervical trunk that originates from the subclavian
artery. It courses superiorly along the anterior scalene muscle and then it turns medially traveling
behind the carotid sheath with variable relationship
to the sympathetic chain. It then turns sharply and
descends on the posterior surface of the lateral lobes
where it forms two branches before entering the inferior pole (Rossi et al., 1971; Hoyes and Kershaw,
1985). Inferior thyroid artery branches in addition to
supplying the thyroid provide blood supply to the
upper esophagus, trachea, and the parathyroid
glands (Monfared et al., 2002). After branching to
anterior and posterior branches, the relationship of
the inferior thyroid artery and the recurrent laryngeal nerve is quite variable and will be discussed
later. Anomalous origin of the inferior thyroid artery
from the vertebral artery and directly from the subclavian artery has been observed, and it was noted
to be absent in 6% of the cases (Daseler and Anson,
1959; Hoyes and Kershaw, 1985).
Thyroidea ima artery is an inconsistent branch in
the arterial supply to the thyroid gland. It has a variable origin and may arise from the aortic arch, subclavian, brachiocephalic trunk, common carotid artery,
or the internal thoracic arteries (ITA) (Hoyes and Kershaw, 1985; Yilmaz et al., 1993; Moriggl and Sturm,
1996). In one study, thyroidea ima artery was identified in 16.9% of the cases (Vasovic et al., 2004).
Although this is a small vessel, on occasion, it may
replace the inferior thyroid artery and become a major
arterial supply to the gland (Hoyes and Kershaw,
1985). It courses superiorly anterior to the trachea to
supply the gland near the midline, and for this reason,
it is in danger of injury during tracheostomy.
VENOUS ANATOMY
Thyroid veins are reported to be a major source of
hemorrhage not only during the thyroid surgery but
during tracheostomies (Krausen, 1976). The dense
plexus of vessels as they pass through the connective tissue of the lobules join under the capsule of
the thyroid and give rise to the superior, middle, and
inferior thyroid veins.
In a study of 30 adult human cadavers, the superior
thyroid vein was present in all samples on both sides.
They noted a single vessel in 83.3% and double vessels in 16.7% of the cases (Wafae et al., 2008). It terminated directly at the internal jugular vein in 52.1%
cases, with linguofacial trunk in 35.4% and with facial
vein in 2.1% of the cases, and it was located at a
plane between 1 and 2.5 cm below the upper margin
of the hyoid bone (Wafae et al., 2008). The middle
thyroid vein in the majority of the cases originates
from the middle third of the thyroid gland from a lateral or posterior position (Dionigi et al., 2010). In a
study of 394 consecutive thyroid surgeries, the prevalence of middle thyroid vein was 62% in the operated
patients with a significant asymmetry between the
sides. The presence of the middle thyroid vein was
more frequent on the right side; however, there were
no significant differences in the origin, caliber, and
length between the two sides (Dionigi et al., 2010). In
another study, the middle thyroid vein drained the
medial part of the gland in 70.4%, the medial and the
lower part in 22.2%, and the upper, medial, and lower
part in 7.4% of the subjects (Wafae et al., 2008). The
inferior thyroid veins and their tributaries are thought
as the ‘‘guardians’’ of the cervical trachea and a
source of massive hemorrhage during emergency tracheostomy (Krausen, 1976). As it arises from within
the body of the thyroid, it communicates with the middle and superior thyroid veins and forms a plexus
behind the sternothyroid muscle in front of the trachea (Belli et al., 1988). The inferior thyroid vein is
reported to be present in 90–97% of the cases (Belli
et al., 1988; Wafae et al., 2008). The number of the
veins are quite variable and up to five veins have been
reported (Wafae et al., 2008). In one study, the termination of the inferior thyroid vein occurred in the right
brachiocephalic vein in 26.1% of the cases, 60.9% in
the left brachiocephalic, and 13% in both vessels
(Wafae et al., 2008). In a computed tomographic
study of the inferior thyroid veins, in up to 60% of the
cases, the veins join to form a single trunk terminating
in the proximal part of the left innominate vein (Belli
et al., 1988).
LYMPHATIC DRAINAGE
The lymphatic drainage of the thyroid gland parallels the venous drainage. The lymphatic channels
Thyroid and Parathyroid Glands and Neurovascular Relations
that accompany the superior and the middle veins
drain into the upper deep nodes of the cervical chain.
Additionally, Rouviere demonstrated a lymphatic
pathway directly connecting the posterior part of the
thyroid lobe to the parapharyngeal and retropharyngeal space in 20% of his dissections (Rouvière,
1932). Although parapharyngeal metastasis from
thyroid carcinoma is rare, it has been reported (Lombardi et al., 2004) and should be recognized as a
pattern of dissemination for thyroid cancer. The lymphatic channels draining with the inferior vessels
drain to the lower nodes of the cervical plexus, supraclavicular, paratracheal, and parapharyngeal
nodes (Hoyes and Kershaw, 1985). Understanding
the pattern of nodal drainage is particularly important in managing patients with thyroid cancer since
the cervicocentral compartment is shown to be most
commonly involved in metastatic thyroid cancer
(Gimm et al., 1998). The lymphatic system of the
thyroid is said to be more developed in young subjects than old, and with increasing age the number
of interfollicular capillaries are reduced and the plexuses formed by them become less dense (Semeina,
1966).
NERVES ASSOCIATED WITH THE
THYROID GLAND—EMBRYOLOGIC
CONSIDERATIONS
The anatomy of the vagus nerve as we know it
today was described by Vesalius and Willis in the
16th and 17th centuries (Steinberg et al., 1986).
The cervical branches of vagus that are pertinent to
thyroid surgery are recurrent laryngeal nerve (RLN)
and superior laryngeal nerves, both the external
branch and the internal branch.
The vagus nerve originates from the medulla
oblongata and exits the skull through the pars nervosa of the jugular foramen. The superior ganglion
(jugular ganglion) of the vagus nerve is located
within the jugular foramen, whereas the nodose ganglion or the inferior ganglion lies just below the foramen (Randolph, 2003). Just below this ganglion is
the takeoff point of the superior laryngeal nerves
(SLN). The vagus descends in the carotid sheath in
the neck initially at a location medial to the internal
jugular and subsequently at a posterior position
between the internal jugular vein and internal carotid
artery inferiorly (Randolph, 2003). The recurrent laryngeal nerves arise as the vagus courses anteriorly
to the aortic arches. As the heart and the great vessels descend during the embryonic development and
the neck elongates, the RLNs get dragged down by
the aortic arches. On the right side, the nerve recurs
around the fourth arch which is the right subclavian
artery, while on the left, the nerve recurs around the
sixth arch which is the ligamentum arteriosum
(Sadler and Langman, 2006).
RECURRENT LARYNGEAL NERVE
The incidence of RLN injury during thyroidectomy
is reported from 0% to 28% (Lahey and Hoover,
25
1938; Simon, 1957; Parnell and Brandenburg, 1970;
Riddell, 1973; Dackiw et al., 2002; Eltzschig et al.,
2002; Marcus et al., 2003). For this reason, recognizing reliable landmarks that will help identify the
location of the RLN during surgery is crucial for its
protection. It is classically identified in the Simon triangle during thyroid surgery formed by the esophagus medially, carotid artery laterally and inferior thyroid artery superiorly (Simon, 1943).
The RLN innervate the intrinsic muscles of the larynx and provide sensory innervation to the glottic
larynx. The right RLN as it curves around the right
subclavian artery, enters the base of the neck at a
more lateral position and its course is less predictable compared to the left RLN (Fig. 1) (Hunt et al.,
1968). They ascend superiorly and medially toward
the tracheoesophageal (TE) groove giving rise to the
tracheal and esophageal branches (Miller, 2003).
The approximate length of the left RLN from the
aorta to the cricothyroid joint is about 12 cm,
whereas the length of the right RLN from the subclavian to the cricothyroid joint is about 5–6 cm (Weisberg et al., 1997). The right RLN is generally not
found within the TE groove until it approaches the
cricothyroid joint (Myssiorek, 2004). The RLN enters
the larynx deep to the inferior constrictor muscle and
posterior to the cricothyroid joint (Myssiorek, 2004).
In a cadaver study by Steinberg et al., it was found
that the inferior third of the left RLN ascends toward
the TE groove a few millimeters lateral to it, but the
right RLN was much more lateral to the groove
(Steinberg et al., 1986). The nerve divides into an
external branch providing motor function to four
intrinsic laryngeal muscles except the cricothyroid
muscle and an internal branch supplying sensation
to the vocal cords and the subglottic region (Ardito
et al., 2004). The RLN in the neck is supplied by the
branches of the ITA that supply part of the trachea
and esophagus. The distal part of the RLN is supplied
by a branch of inferior laryngeal artery which itself is
a branch of ITA (Monfared et al., 2002). The variable
relationship of the RLN to the TE groove, ligament of
Berry, and inferior thyroid artery had been described
by many surgeons and anatomists (Bliss et al.,
2000; Reeve and Thompson, 2000; Ardito et al.,
2004). However, the nerve generally passes posterior to the middle thyroid vein (Bachhuber, 1943).
Variation in the pattern of distal bifurcation of the
RLN has also been reported (Nemiroff and Katz,
1982; Katz, 1986). In a study by Nemiroff et al., a
total of 153 recurrent laryngeal nerves were
observed of which 41.2% bifurcated or trifurcated
into extralaryngeal branches with varying sizes
(Nemiroff and Katz, 1982). They noted four instances of trifurcations. In a study of 1177 RLN observed
in 719 patients, 63% bifurcated or trifurcated over
0.5 cm inferior to the cricoid cartilage. Of these, 170
patients had bilateral nerve bifurcations (Katz and
Nemiroff, 1993). In a study of 721 RLNs, 58% bifurcated or trifurcated more than 0.5 cm form the cricoid cartilage (Katz, 1986). Rusted and Morrison in
their study of 100 cadaveric dissections noticed a
high variability in the level of division of the main
trunks of the RLN and the size of the branches
(Rustad and Morrison, 1952). Functional studies of
26
Mohebati and Shaha
the extra laryngeal nerve branches demonstrated
that motor branches to both the abductor and
adductor muscles of the larynx are in the anterior division (Serpell et al., 2009). During thyroid surgery,
identification and preservation of the recurrent laryngeal nerve and all of its divisions is essential to
decrease the morbidity of the procedure.
The relationship of the distal segment of the RLN
to the cricothyroid joint has been reported to be
more constant coursing just posterior to the joint. In
a review of 278 RLNs dissected in 190 patients by
Shindo et al. during thyroidectomy, the course of the
distal portion of the nerve to a line parallel to the TE
groove was recorded. They recorded that 78% of the
right-sided nerves coursed between 15 and 45
degrees, and 77% of the left-sided nerves coursed
between 0 and 30 degrees (Shindo et al., 2005). The
authors concluded that identifying the nerve distally
may be more reliable with less chance of disrupting
the blood supply to the RLN.
The course of RLN with respect to interior thyroid
artery is quite variable but significant (Fig. 3). In a
cadaveric study of 50 specimens, 100 RLNs and 96
inferior thyroid arteries (ITA) were identified. The
author observed 20 various configurations according
to the location of the main trunk of the nerve and its
branches entering the larynx. On the right, the nerve
was frequently in front of the artery, and on the left
the nerve was often behind the 2 branches of the artery (Yalcin, 2006). In another study of cadavers, in
75% of the cases, branches of the RLN formed a
delta–delta interjunction with the branches of the ITA
without any constant anatomical relationship between
the two structures (Steinberg et al., 1986). In a study
of 172 thyroidectomies by Lekacos et al., 191 RLNs
were identified. 82.6% of the left and 85.4% of right
RLN ran either posterior or in between the branches
of the ITA and only a small percentage coursing anterior to the artery. The majority of the nerves were
found within 3 mm of the Berry’s ligament. The
authors concluded that the relationship of the RLN to
ITA and Berry’s ligament does not follow a constant
anatomical pattern (Lekacos et al., 1992).
The recurrent RLN lays in close proximity the posterior suspensory ligament as described by Berry in
1888 (Proceedings of the Anatomical Society of
Great Britain and Ireland, 1888). It is described to
be embedded or lateral to the suspensory ligament
(Lore, 1983; Leow and Webb, 1998; Sasou et al.,
1998). In a cadaveric study by Leow and Webb at
the level of the cricoid cartilage, the mean distance
between the attachment of the ligament to the cricoid cartilage and the RLN entry point into the larynx
was 1.9 mm (Leow and Webb, 1998). In another
study of 689 RLNs, all nerves were located dorsolaterally to the ligament of Berry and no nerve penetrated the ligament (Sasou et al., 1998).
Tubercle of Zukerkandl is another landmark that
can be useful in identifying the RLN. In a study of 104
lobectomies by Pelizzo et al. the tubercle of Zukerkandl was identified in 78.2% of the lobectomies on
the right and 75.5% of the cases on the left. The
authors concluded that identifying this tubercle will
make identification of RLN easier (Pelizzo et al., 1998).
NON-RECURRENT LARYNGEAL NERVE
During the embryologic development, when a segment of the fourth right aortic arch between the right
common carotid and right subclavian disappears, it
results in a break in the primitive arterial rings. The
break in the ring leads to the formation of a left aortic arch and the right subclavian artery take off
below the left subclavian artery (Mra and Wax,
1999; Randolph, 2003; Sadler and Langman, 2006).
Due to this aberrant take off, the right subclavian artery must cross the midline behind the esophagus to
reach the right arm (Myssiorek, 2004). This may
cause compression of the esophagus and result in
dysphagia. As a consequence of this atresia, the
innominate artery is absent under which the right
RLN loops to ascend in the neck. Therefore the right
RLN arises from the vagus in the cervical region
(Sanders et al., 1983; Randolph, 2003). Depending
on its point of origin, the non-recurrent laryngeal
nerve courses inferiorly along the vagus usually
passing behind the common carotid artery. It can
arise at the level of the thyroid cartilage or the superior thyroid pole and pass directly to the larynx (Fig.
4) (Stewart et al., 1972). It is also reported to arise
at the level of the inferior thyroid artery, passing to
the TE groove at the level of the inferior pole of the
thyroid gland and then following the normal course
of the RLN (Stewart et al., 1972). Henry et al.
observed 31 cases of right nonrecurrent laryngeal
nerve in 4,921 dissections (0.63%). Additionally,
they identified left-sided nonrecurrent laryngeal
nerve in two cases out of 4,673 dissections (0.04%);
however, both patients had a right aortic arch associated with situs inversus (Henry et al., 1988). In
another series of 1,000 consecutive thyroidectomies,
seven cases (0.7%) of nonrecurrent laryngeal nerve
on the right was identified (Sanders et al., 1983).
Preoperative diagnosis of nonrecurrent laryngeal
nerve by identifying an aberrant right subclavian artery or ‘‘arteria lusoria’’ using ultrasonography and
computed tomography has been reported and may
be beneficial for operative planning (Watanabe et
al., 2001; Hermans et al., 2003; Iacobone et al.,
2008; Wang et al., 2010). Another source of pitfall
during the thyroid surgery is the communicating
branches between the cervical sympathetic system
and the recurrent laryngeal nerve (Steinberg et al.,
1986; Sato et al., 1997; Raffaelli et al., 2000). These
branches may arise from the middle cervical chain
ganglion, inferior cervical chain ganglion, or superior
cardiac nerve. In a series of 656 right-sided dissections, a nonrecurrent laryngeal nerve was identified
in 0.45% and a sympathetic recurrent laryngeal
nerve anastomotic branch was identified in 10 cases
(1.5%) (Raffaelli et al., 2000). These branches could
be large with similar diameter to the RLN and can be
mistaken for the nonrecurrent laryngeal nerve during
thyroid surgery and neck dissection.
SUPERIOR LARYNGEAL NERVE
The superior laryngeal nerve (SLN) is one of the
first branches of vagus separating at the nodose
Thyroid and Parathyroid Glands and Neurovascular Relations
27
Fig. 4. Anatomic variation in the course of the nonrecurrent laryngeal nerve as it
travels along the inferior thyroid artery (A) or directly to the larynx at the level of the
superior pole of the thyroid (B). Reprinted with permission from Stewart et al. (1972).
ganglion about 4 cm from the carotid bifurcation and
descending posteriorly and medial to the carotid
sheath (Kierner et al., 1998; Randolph, 2003). During this descent, it passes anterior to the superior
sympathetic cervical ganglion (Kambic et al., 1984;
Monfared et al., 2002). In about 1.5 cm inferiorly,
the SLN divides into the internal and external
branches (Kambic et al., 1984; Randolph, 2003). In
a cadaveric study of 50 subjects, about 6% of the
SLN bifurcations occurred at the origin of the nerve
with a mean length of 16.7 mm (Furlan et al.,
2003).
Understanding the relationship of the external
branch of the superior laryngeal nerve (EBSLN) to
the upper pole of the thyroid and the STA is crucial
in safeguarding this nerve during surgery. (Aluffi et
al., 2001). The presenting symptoms of injury to the
EBSLN are hoarseness, decreased pitch, or volume,
and voice fatigue. Laryngeal electromyography is the
gold standard for evaluation and diagnosis of EBSLN
injury (Sulica, 2004). The EBSLN sends motor fibers
to the cricothyroid muscle and innervate parts of the
intralaryngeal mucous membrane (Moran and Castro, 1951). It courses anteriorly and inferiorly with
variable course along the inferior pharyngeal constrictor muscles and the branches of superior thyroid
artery (Teitelbaum and Wenig, 1995). It curves
anteriorly and medially close to the lower edge of the
thyroid cartilage before innervating of the cricothy-
roid muscle (Furlan et al., 2003). The EBSLN almost
invariably approaches the larynx within the sternothyrolaryngeal (Joll’s) triangle. The limits of this
triangle are the inferior laryngeal constrictor and cricothyroid muscle medially, sternothyroid muscle
anteriorly, and superior thyroid pole anteriorly
(Randolph, 2003). For safeguarding the EBSLN during surgical procedures, knowledge of the anatomy
of this nerve as it relates to the superior thyroid pole
and vessels is essential (Fig. 5). In a cadaveric study
of 31 subjects by Kierner et al., four types of relationship between the EBSLN and the upper pole of
the thyroid and STA was noted. In 42% of the cases,
EBSLN crossed STA more than 1 cm above the upper
pole of the thyroid, in 30% within 1 cm of the upper
pole and in the remaining 28%, EBSLN crossed
under the cover of the upper pole or immediately
above the upper pole of the thyroid gland (Kierner et
al., 1998). In another study by Cernea at al., in 15
cadavers, 60% of the EBSLN were identified more
than 1 cm above the upper pole of the thyroid, 17%
less than 1 cm and in 20% crossing the vessels
below the upper pole of the thyroid (Cernea et al.,
1992). Based on these two studies and others with
similar classification method, EBSLN is at risk for
injury in 37% to 72% thyroid surgeries (HurtadoLopez and Zaldivar-Ramirez, 2002). The rate of
injury to the EBSLN is reported between 0 and 58%
and is likely underreported.
28
Mohebati and Shaha
Fig. 5. The variation in the course of the external
branch of the superior laryngeal nerve with respect to
the superior thyroid artery and superior thyroid pole. A:
The EBSLN descends superficial to the inferior constrictor muscle (IC) along with the superior thyroid vessels
and is visible in its entire course before innervating the
cricothyroid (CT) muscle. B: The EBSLN pierces the IC
muscle about 1 cm above the CT membrane (arrow). C:
The EBSLN runs deep to the IC muscle and is protected.
CP marks the cricopharyngeus muscle. (Courtesy of the
Memorial Sloan-Kettering Cancer Center, New York, NY;
with permission.) [Color figure can be viewed in the
online issue, which is available at wileyonlinelibrary.
com.]
The internal branch of the superior laryngeal
nerve (IBSLN) pierces the thyrohyoid membrane in
association with the superior thyroid artery (Sulica,
2004). It supplies the sensory innervation to the mucosa of the larynx. The IBSLN is divided into three
divisions: the superior, middle, and inferior divisions
(Sanders and Mu, 1998; Sulica, 2004). The superior
division supplies the mucosa of the laryngeal surface
of the epiglottis. The middle division supplies the
mucosa of the true and false vocal folds and the
aryepiglottic fold, and the inferior division supplies
the mucosa of the arytenoid region, subglottis, anterior wall of the hypopharynx, and upper esophageal
sphincter (Sanders and Mu, 1998). It has been suggested that some of the fibers of the IBSLN provide
motor innervation to the interarytenoid muscle (Wu
et al., 1994; Sanders and Mu, 1998).
has allowed for improving the operative technique
with each step aimed at preserving the integrity and
the function of these structures. The correct knowledge of the anatomic variations of the thyroid,
parathyroid glands, and the regional neurovascular
anatomy is essential for performing safe and uncomplicated operations.
CONCLUSION
Over the course of last century, thyroid surgery
has evolved from an operation with high morbidity
and mortality into a much safer operation with low
morbidity in experienced hands. Extensive studies
performed by anatomists and surgeons to define the
anatomy of the thyroid and parathyroid glands and
the surrounding neurovascular structures have been
instrumental in this progress. This understanding
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