2314703код для вставки
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 REFERENCES 1888. Proceedings of the Anatomical Society of Great Britain and Ireland. J Anat Physiol 22:xix–xxix. Akerstrom G, Malmaeus J, Bergstrom R. 1984. Surgical anatomy of human parathyroid glands. Surgery 95:14–21. Akyol MU, Koc C, Ozcan M, Ozdem C. 1997. Superior thyroid artery arising from the common carotid artery. Otolaryngol Head Neck Surg 116:701. Alufﬁ P, Policarpo M, Cherovac C, Olina M, Dosdegani R, Pia F. 2001. Post-thyroidectomy superior laryngeal nerve injury. Eur Arch Otorhinolaryngol 258:451–454. Alveryd A. 1968. Parathyroid glands in thyroid surgery. I. Anatomy of parathyroid glands. II. Postoperative hypoparathyroidism— Identiﬁcation and autotransplantation of parathyroid glands. Acta Chir Scand 389:1–120. Ardito G, Revelli L, D’Alatri L, Lerro V, Guidi ML, Ardito F. 2004. Revisited anatomy of the recurrent laryngeal nerves. Am J Surg 187:249–253. Arriaga MA, Myers EN. 1988. Ectopic thyroid in the retroesophageal superior mediastinum. Otolaryngol Head Neck Surg 99:338–340. Thyroid and Parathyroid Glands and Neurovascular Relations Bachhuber CA. 1943. Complications of thyroid surgery. Anatomy of the recurrent laryngeal nerve, middle thyroid vein and inferior thyroid artery. Am J Surg 60:5. Bahar G, Feinmesser R, Joshua BZ, Shpitzer T, Morgenstein S, Popovtzer A, Shvero J. 2006. Hyperfunctioning intrathyroid parathyroid gland: a potential cause of failure in parathyroidectomy. Surgery 139:821–826. Belli AM, Ingram CE, Heron CW, Husband JE. 1988. The appearance of the inferior thyroid veins on computed tomography. Br J Radiol 61:125–127. Bliss RD, Gauger PG, Delbridge LW. 2000. Surgeon’s approach to the thyroid gland: surgical anatomy and the importance of technique. World J Surg 24:891–897. Bowen-Wright HE, Jonklaas J. 2005. Ectopic intratracheal thyroid: An illustrative case report and literature review. Thyroid 15:478–484. Braun EM, Windisch G, Wolf G, Hausleitner L, Anderhuber F. 2007. The pyramidal lobe: Clinical anatomy and its importance in thyroid surgery. Surg Radiol Anat 29:21–27. Cernea CR, Ferraz AR, Nishio S, Dutra A Jr, Hojaij FC, dos Santos LR. 1992. Surgical anatomy of the external branch of the superior laryngeal nerve. Head Neck 14:380–383. Chan JK, Rosai J. 1991. Tumors of the neck showing thymic or related branchial pouch differentiation: a unifying concept. Hum Pathol 22:349–367. Dackiw AP, Rotstein LE, Clark OH, 2002. Computer-assisted evoked electromyography with stimulating surgical instruments for recurrent/external laryngeal nerve identiﬁcation and preservation in thyroid and parathyroid operation. Surgery 132:1100– 1106; discussion 1107–1108. Daseler EH, Anson BJ. 1959. Surgical anatomy of the subclavian artery and its branches. Surg Gynecol Obstet 108:149–174. DeGroot LJ, Larsen PR, Hennemann G. 1996. The thyroid and its diseases, 6th Ed. New York: Churchill Livingstone. Dionigi G, Congiu T, Rovera F, Boni L. 2010. The middle thyroid vein: anatomical and surgical aspects. World J Surg 34:514– 520. Eltzschig HK, Posner M, Moore FD Jr. 2002. The use of readily available equipment in a simple method for intraoperative monitoring of recurrent laryngeal nerve function during thyroid surgery: Initial experience with more than 300 cases. Arch Surg 137:452– 456; discussion 456–457. Fancy T, Gallagher D 3rd, Hornig JD. 2010. Surgical anatomy of the thyroid and parathyroid glands. Otolaryngol Clin North Am 43:221–227,vii. Ferlito A, Giarelli L, Silvestri F. 1988. Intratracheal thyroid. J Laryngol Otol 102:95–96. Furlan JC, Brandao LG, Ferraz AR, Rodrigues AJ Jr., 2003. Surgical anatomy of the extralaryngeal aspect of the superior laryngeal nerve. Arch Otolaryngol Head Neck Surg 129:79–82. Gimm O, Rath FW, Dralle H. 1998. Pattern of lymph node metastases in papillary thyroid carcinoma. Br J Surg 85:252–254. Goodman A, Politz D, Lopez J, Norman J. 2011. Intrathyroid parathyroid adenoma: Incidence and location—The case against thyroid lobectomy. Otolaryngl Head Neck Surg 144:867–871. Gray SW, Skandalakis JE, Akin JT Jr. 1976. Embryological considerations of thyroid surgery: Developmental anatomy of the thyroid, parathyroids and the recurrent laryngeal nerve. Am Surg 42:621–628. Halsted WS, Evans HM. 1907. The parathyroid glandules. I. Their blood supply and their preservation in operation upon the thyroid gland. Ann Surg 46:489–506. Hanbury EM Jr, Boyd DP. 1963. History of thyroid surgery. Surgery 54:550–556. Harjeet A, Sahni D, Jit I, Aggarwal AK. 2004. Shape, measurements and weight of the thyroid gland in Northwest Indians. Surg Radiol Anat 26:91–95. Hegner CF. 1932. A history of thyroid surgery. Ann Surg 95:481– 492. Henry JF, Audiffret J, Denizot A, Plan M. 1988. The nonrecurrent inferior laryngeal nerve: Review of 33 cases, including two on the left side. Surgery 104:977–984. 29 Hermans R, Dewandel P, Debruyne F, Delaere PR. 2003. Arteria lusoria identiﬁed on preoperative CT and nonrecurrent inferior laryngeal nerve during thyroidectomy: a retrospective study. Head Neck 25:113–117. Hollinshead WH. 1968. Anatomy for Surgeons. 2nd Ed. New York/ London: Hoeber Medical. Hoyes AD, Kershaw DR. 1985. Anatomy and development of the thyroid gland. Ear Nose Throat J 64:318–333. Hunt PS, Poole M, Reeve TS. 1968. A reappraisal of the surgical anatomy of the thyroid and parathyroid glands. Br J Surg 55:63–66. Hurtado-Lopez LM, Zaldivar-Ramirez FR. 2002. Risk of injury to the external branch of the superior laryngeal nerve in thyroidectomy. Laryngoscope 112:626–629. Iacobone M, Viel G, Zanella S, Bottussi M, Frego M, Favia G. 2008. The usefulness of preoperative ultrasonographic identiﬁcation of nonrecurrent inferior laryngeal nerve in neck surgery. Langenbecks Arch Surg 393:633–638. Ito Y, Miyauchi A, Nakamura Y, Miya A, Kobayashi K, Kakudo K. 2007. Clinicopathologic signiﬁcance of intrathyroidal epithelial thymoma/carcinoma showing thymus-like differentiation: A collaborative study with Member Institutes of The Japanese Society of Thyroid Surgery. Am J Clin Pathol 127:230–236. Kamat MR, Kulkarni JN, Desai PB, Jussawalla DJ. 1979. Lingual thyroid: A review of 12 cases. Br J Surg 66:537–539. Kambic V, Zargi M, Radsel Z. 1984. Topographic anatomy of the external branch of the superior laryngeal nerve. Its importance in head and neck surgery. J Laryngol Otol 98:1121–1124. Kaplan EL, Yashiro T, Salti G. 1992. Primary hyperparathyroidism in the 1990s. Choice of surgical procedures for this disease. Ann Surg 215:300–317. Katz AD. 1986. Extralaryngeal division of the recurrent laryngeal nerve. Report on 400 patients and the 721 nerves measured. Am J Surg 152:407–410. Katz AD, Nemiroff P. 1993. Anastamoses and bifurcations of the recurrent laryngeal nerve—Report of 1177 nerves visualized. Am Surg 59:188–191. Kierner AC, Aigner M, Burian M. 1998. The external branch of the superior laryngeal nerve: Its topographical anatomy as related to surgery of the neck. Arch Otolaryngol Head Neck Surg 124:301–303. Krausen AS. 1976. The inferior thyroid veins–the ultimate guardians of the trachea. Laryngoscope 86:1849–1855. Kurtay M, Crile G Jr. 1969. Aberrant parathyroid glands in relationship to the thymus. Am J Surg 117:705. Lahey FH, Hoover WB. 1938. Injuries to the recurrent laryngeal nerve in thyroid operations: Their management and avoidance. Ann Surg 108:545–562. Larsen WJ, Sherman LS, Potter SS, Scott WJ. 2001. Human Embryology. 3rd Ed. New York: Churchill Livingstone. Lehr RP Jr. 1979. Musculus levator glandulae thyroideae: An observation. Anat Anz 146:494–496. Lekacos NL, Tzardis PJ, Sﬁkakis PG, Patoulis SD, Restos SD. 1992. Course of the recurrent laryngeal nerve relative to the inferior thyroid artery and the suspensory ligament of Berry. Int Surg 77:287–288. Leow CK, Webb AJ. 1998. The lateral thyroid ligament of Berry. Int Surg 83:75–78. Levy HA, Sziklas JJ, Rosenberg RJ, Spencer RP. 1982. Incidence of a pyramidal lobe on thyroid scans. Clin Nucl Med 7:560–561. Lombardi D, Nicolai P, Antonelli AR, Maroldi R, Farina D, Shaha AR. 2004. Parapharyngeal lymph node metastasis: An unusual presentation of papillary thyroid carcinoma. Head Neck 26:190– 196. Lore JM Jr. 1983. Practical anatomical considerations in thyroid tumor surgery. Arch Otolaryngol 109:568–574. Loukas M, Merbs W, Tubbs RS, Curry B, Jordan R. 2008. Levator glandulae thyroideae muscle with three slips. Anat Sci Int 83:273–276. Mansberger AR Jr, Wei JP. 1993. Surgical embryology and anatomy of the thyroid and parathyroid glands. Surg Clin North Am 73:727–746. 30 Mohebati and Shaha Marcus B, Edwards B, Yoo S, Byrne A, Gupta A, Kandrevas J, Bradford C, Chepeha DB, Teknos TN. 2003. Recurrent laryngeal nerve monitoring in thyroid and parathyroid surgery: The University of Michigan experience. Laryngoscope 113:356–361. Marshall CF. 1895. Variations in the form of the thyroid gland in man. J Anat Physiol 29:234–239. Massine RE, Durning SJ, Koroscil TM. 2001. Lingual thyroid carcinoma: a case report and review of the literature. Thyroid 11: 1191–1196. Mete O, Rotstein L, Asa SL. 2010. Controversies in thyroid pathology: thyroid capsule invasion and extrathyroidal extension. Ann Surg Oncol 17:386–391. Miller FR. 2003. Surgical anatomy of the thyroid and parathyroid glands. Otolaryngol Clin North Am 36:1–7;vii. Monfared A, Gorti G, Kim D. 2002. Microsurgical anatomy of the laryngeal nerves as related to thyroid surgery. Laryngoscope 112:386–392. Moran RE, Castro AF. 1951. The superior laryngeal nerve in thyroid surgery. Ann Surg 134:1018–1021. Moriggl B, Sturm W. 1996. Absence of three regular thyroid arteries replaced by an unusual lowest thyroid artery (A. thyroidea ima): A case report. Surg Radiol Anat 18:147–150. Mra Z, Wax MK. 1999. Nonrecurrent laryngeal nerves: anatomic considerations during thyroid and parathyroid surgery. Am J Otolaryngol 20:91–95. Myers EN, Pantangco IP Jr. 1975. Intratracheal thyroid. Laryngoscope 85:1833–1840. Myssiorek D. 2004. Recurrent laryngeal nerve paralysis: anatomy and etiology. Otolaryngol Clin North Am 37:25–44;v. Neinas FW, Gorman CA, Devine KD, Woolner LB. 1973. Lingual thyroid. Clinical characteristics of 15 cases. Ann Intern Med 79: 205–210. Nemiroff PM, Katz AD. 1982. Extralaryngeal divisions of the recurrent laryngeal nerve. Surgical and clinical signiﬁcance. Am J Surg 144:466–469. Noyek AM, Friedberg J. 1981. Thyroglossal duct and ectopic thyroid disorders. Otolaryngol Clin North Am 14:187–201. Organ GM, Organ CH Jr. 2000. Thyroid gland and surgery of the thyroglossal duct: Exercise in applied embryology. World J Surg 24:886–890. Parnell FW, Brandenburg JH. 1970. Vocal cord paralysis. A review of 100 cases. Laryngoscope 80:1036–1045. Pelizzo MR, Toniato A, Gemo G. 1998. Zuckerkandl’s tuberculum: An arrow pointing to the recurrent laryngeal nerve (constant anatomical landmark). J Am Coll Surg 187:333–336. Proye C, Bizard JP, Carnaille B, Quievreux JL. 1994. [Hyperparathyroidism and intrathyroid parathyroid gland. 43 cases]. Ann Chir 48:501–506. Raffaelli M, Iacobone M, Henry JF. 2000. The ‘‘false’’ nonrecurrent inferior laryngeal nerve. Surgery 128:1082–1087. Ranade AV, Rai R, Pai MM, Nayak SR, Prakash Krisnamurthy A, Narayana S. 2008. Anatomical variations of the thyroid gland: possible surgical implications. Singapore Med J 49:831–834. Randolph G. 2003. Surgery of the thyroid and parathyroid glands. Philadelphia, PA; [London]: Saunders. Reeve T, Thompson NW. 2000. Complications of thyroid surgery: How to avoid them, how to manage them, and observations on their possible effect on the whole patient. World J Surg 24:971–975. Riddell V. 1973. The recurrent laryngeal nerve and thyroidectomy. Lancet 1:1190. Rossi P, Tracht DG, Ruzicka FF. 1971. Thyroid angiography—Techniques, anatomy and indications. Br J Radiol 44:911–926. Rouvière H. 1932. Anatomie des lymphatiques de l’homme. Paris: Masson et Cie. Rubenfeld S, Joseph UA, Schwartz MR, Weber SC, Jhingran SG. 1988. Ectopic thyroid in the right carotid triangle. Arch Otolaryngol Head Neck Surg 114:913–915. Rustad WH, Morrison LF. 1952. Revised anatomy of the recurrent laryngeal nerves. Surgical importance based on the dissection of 100 cadavers: A preliminary report. Laryngoscope 62:237–249. Sadler TW, Langman J. 2006. Langman’s Medical Embryology. 10th Ed. Philadelphia, PA: Lippincott Williams & Wilkins. Sanders G, Uyeda RY, Karlan MS. 1983. Nonrecurrent inferior laryngeal nerves and their association with a recurrent branch. Am J Surg 146:501–503. Sanders I, Mu L. 1998. Anatomy of the human internal superior laryngeal nerve. Anat Rec 252:646–656. Sasou S, Nakamura S, Kurihara H. 1998. Suspensory ligament of Berry: Its relationship to recurrent laryngeal nerve and anatomic examination of 24 autopsies. Head Neck 20:695–698. Sato I, Sato T, Shimada K. 1997. Communication between the superior cervical sympathetic ganglion and the inferior laryngeal nerve. J Anat 190(Pt 1):147–148. Sauk JJ Jr. 1970. Ectopic lingual thyroid. J Pathol 102:239–243. Savage PE, Khan O, Grover S, Ott R, McCready VR. 1984. The appearance of the pyramidal lobe on thyroid scintigraphy. Nucl Med Commun 5:163–168. Semeina NA. 1966. Lymphatic system in thyroid gland at different ages. Fed Proc Transl Suppl 25:669–671. Serpell JW, Yeung MJ, Grodski S. 2009. The motor ﬁbers of the recurrent laryngeal nerve are located in the anterior extralaryngeal branch. Ann Surg 249:648–652. Shindo ML, Wu JC, Park EE. 2005. Surgical anatomy of the recurrent laryngeal nerve revisited. Otolaryngol Head Neck Surg 133:514– 519. Simon MM. 1943. Recurrent laryngeal nerve in thyroid surgery. Triangle for its recognition and protection. Am J Surg 60:9. Simon MM. 1957. Safeguarding the recurrent laryngeal nerve in thyroid surgery: A triangle for its localization and protection. Miss Valley Med J 79:180–186. Smith SD, Benton RS. 1978. A rare origin of the superior thyroid artery. Acta Anat (Basel) 101:91–93. Steinberg JL, Khane GJ, Fernandes CM, Nel JP. 1986. Anatomy of the recurrent laryngeal nerve: a redescription. J Laryngol Otol 100:919–927. Stewart GR, Mountain JC, Colcock BP. 1972. Non-recurrent laryngeal nerve. Br J Surg 59:379–381. Strickland AL, Macﬁe JA, Van Wyk JJ, French FS. 1969. Ectopic thyroid glands simulating thyroglossal duct cysts. Hypothyroidism following surgical excision. JAMA 208:307–310. Sturniolo G, Bonanno L, Gagliano E, Tonante A, Taranto F, Mamo M, De Salvo G, Sturnioloa G. 2008. [The thyroid pyramidal lobe: Frequency, morphological features and related diseases]. Chir Ital 60:41–46. Sugiyama S. 1971. The embryology of the human thyroid gland including ultimobranchial body and others related. Ergeb Anat Entwicklungsgesch 44:3–111. Sulica L. 2004. The superior laryngeal nerve: Function and dysfunction. Otolaryngol Clin North Am 37:183–201. Teitelbaum BJ, Wenig BL. 1995. Superior laryngeal nerve injury from thyroid surgery. Head Neck 17:36–40. Vasovic L, Arsic S, Vlajkovic S, Zdravkovic D. 2004. Morphological aspect of the thyroid ima artery in human fetuses. Ital J Anat Embryol 109:189–197. Vazquez T, Cobiella R, Maranillo E, Valderrama FJ, McHanwell S, Parkin I, Sanudo JR. 2009. Anatomical variations of the superior thyroid and superior laryngeal arteries. Head Neck 31:1078–1085. Wafae N, Hirose K, Franco C, Wafae GC, Ruiz CR, Daher L, Person OC. 2008. The anatomy of the human thyroid veins and its surgical application. Folia Morphol (Warsz) 67:221–225. Wang C. 1976. The anatomic basis of parathyroid surgery. Ann Surg 183:271–275. Wang C. 1981. Hyperfunctioning intrathyroid parathyroid gland: A potential cause of failure in parathyroid surgery. J R Soc Med 74:49–52. Wang Y, Ji Q, Li D, Wu Y, Zhu Y, Huang C, Shen Q, Wang Z, Zhang L, Sun T. 2010. Preoperative CT diagnosis of right nonrecurrent inferior laryngeal nerve. Head Neck 33:232–238. Watanabe A, Kawabori S, Osanai H, Taniguchi M, Hosokawa M. 2001. Preoperative computed tomography diagnosis of non-recurrent inferior laryngeal nerve. Laryngoscope 111:1756–1759. Waters ZJ, McCullough K, Thomas NR. 1953. Lingual thyroid; historical data, developmental anatomy, and report of a case. AMA Arch Otolaryngol 57:60–78. Thyroid and Parathyroid Glands and Neurovascular Relations Weider DJ, Parker W. 1977. Lingual thyroid: Review, case reports, and therapeutic guidelines. Ann Otol Rhinol Laryngol 86:841–848. Weisberg NK, Spengler DM, Netterville JL. 1997. Stretch-induced nerve injury as a cause of paralysis secondary to the anterior cervical approach. Otolaryngol Head Neck Surg 116:317–326. Welsh DA. 1898. Concerning the parathyroid glands: A critical, anatomical, and experimental study. J Anat Physiol 32:292–307. Williams JD, Sclafani AP, Slupchinskij O, Douge C. 1996. Evaluation and management of the lingual thyroid gland. Ann Otol Rhinol Laryngol 105:312–316. Wu BL, Sanders I, Mu L, Biller HF. 1994. The human communicating nerve. An extension of the external superior laryngeal nerve 31 that innervates the vocal cord. Arch Otolaryngol Head Neck Surg 120:1321–1328. Wu SL, Gupta D, Connelly J. 2001. Adult ectopic thymus adjacent to thyroid and parathyroid. Arch Pathol Lab Med 125:842–843. Yalcin B. 2006. Anatomic conﬁgurations of the recurrent laryngeal nerve and inferior thyroid artery. Surgery 139:181–187. Yilmaz E, Celik HH, Durgun B, Atasever A, Ilgi S. 1993. Arteria thyroidea ima arising from the brachiocephalic trunk with bilateral absence of inferior thyroid arteries: a case report. Surg Radiol Anat 15:197–199. Yoon JS, Won KC, Cho IH, Lee JT, Lee HW. 2007. Clinical characteristics of ectopic thyroid in Korea. Thyroid 17:1117–1121.