Thyroid and parathyroid glands

Embryology and congenital anomalies

The thyroid gland appears at about 30–31 days post fertilization (stages 11–12) as a median endodermal thickening in the floor of the primitive pharynx, located between the first and second pharyngeal pouches, which invaginates into the surrounding neural crest mesenchyme. As the lower pharyngeal arches form and the heart descends, the diverticulum extends as the thyroglossal duct, anterior to the developing hyoid bone and laryngeal cartilages. The original site of invagin­ation, the foramen caecum, is located at the junction of the anterior two-thirds (oral portion) and posterior one-third (pharyngeal portion) of the tongue. The thyroid gland is bilobed, forming thyroid lobes and an isthmus by stage 14 (32–34 days post fertilization), and is near the rostral border of the aortic sac at stage 15 (35–36 days post fertilization). As it extends caudally to its pretracheal position, it fuses lat­erally with cells of the caudal pharyngeal complex (fourth pharyngeal pouch and ultimobranchial body) that become incorporated into the lateral aspect of the developing thyroid gland, and is the origin of the calcitonin-secreting parafollicular or ‘C’ cells.

Complete failure of descent of the thyroglossal duct leads to the development of thyroid tissue within the tongue, which is referred to as a lingual thyroid. The persistence of thyroid tissue along its path of migration may also lead to entirely ectopic thyroid glands (sublingual, prelaryngeal and pretracheal glands) or ectopic thyroid tissue deposits, also referred to as small accessory thyroid glands ( Fig. 18.2 ). The surgeon should be aware that an ectopic thyroid gland may easily be mistaken for a thyroglossal duct cyst and if removed will lead to hypothyroidism. Thus, preoperative imaging (radioactive iodine uptake scan or neck ultrasound) should be considered to determine if additional thyroid tissue is present. Persistence of the most distal portion of the thyroglossal duct occurs in approximately 50% of individuals, and gives rise to the pyramidal thyroid lobe and the levator glandulae thyroideae. The pyramidal lobe is a tongue of thyroid tissue extending from the superior border of the isthmus, usually at its junction with the left lobe, towards the hyoid bone, to which it is connected by a fibrous band, the levator glandulae thyroideae, which may contain muscular fibres (see Fig. 18.2 ). During total thyroidectomy, care must be taken to remove the entire pyramidal lobe in order to avoid persistence of an excessively large thyroid remnant. The thyroglossal duct atrophies, but remnants may persist anywhere along its path of migration and lead to the development of a thyroglossal duct cyst (see Fig. 18.2 ). The latter may become infected, require drainage and fistulize through the overlying skin; uncommonly, these cysts may even give rise to thyroid malignancy. During resection of a thyroglossal duct cyst, also referred to as the Sistrunk procedure, the cyst and its associated duct, as well as the central portion of the hyoid bone, are removed en bloc in order to reduce the risk of recurrence. Prelaryngeal lymph nodes may commonly be found along the course of the pyramidal lobe. Calcitonin-producing parafollicular cells, or C cells, arise within the paired ultimobranchial bodies that are derived from the fourth branchial pouch during the fifth week of gestation, and become incorporated into the developing thyroid. The Zuckerkandl tubercle (ZT), a posterolateral projection of the thyroid gland, located adjacent to the junction of the thyroid and cricoid cartilages, is a remnant of the ultimobranchial body. The ZT is present in approximately 70% of individuals and usually is less than 1 cm in diameter. When present, it constitutes a useful anatomical landmark for identification of the RLN and the superior parathyroid gland. The ZT has been described as being shaped like an ‘arrow that points towards the RLN’. This is because the RLN travels posteromedially to a well-developed ZT in more than 80% of people, and in this location the nerve may often be mistaken as travelling intrathyroidally ( Fig. 18.3 ). The RLN may, through gentle dissection and with medial retraction of the ZT, be gradually exposed up to its entry into the larynx. Like the ZT, the superior parathyroid glands are also derived from the fourth pharyngeal pouch; their common embryological origin explains the consistent posterior and superior location of the superior parathyroid gland in relation to the ZT. Thus, the superior parathyroid gland should be routinely identified and its blood supply carefully preserved during thyroidectomy, especially when dissecting the ZT. Midline thyroid tissues that extend inferiorly into the thyrothymic ligament are referred to as thyrothymic thyroid rests (TTR) (see Fig. 18.2 ). TTR also represent remnants of the developing thyroid gland that may be present in more than half of individuals, and during surgery may be mistaken for lymph nodes or parathyroids.

The parathyroid glands develop at about stage 14 (32–34 days post fertilization) as interactions between the dorsal endodermal epithelium and the underlying neural crest mesenchyme of the third and fourth pharyngeal pouches. The ventral epithelium of these pouches gives rise to the thymus and lateral thyroid tissue, respectively. Parathyroid III (inferior parathyroid gland) migrates earlier and moves further caudally than parathyroid IV (superior parathyroid gland), which becomes anchored to the developing lateral lobes of the thyroid gland. This leads to the inferior parathyroids having a more variable location than the superior. Congenital anomalies in parathyroid development include variations in gland number, shape, size, weight, colour, and the development of a cystic component.

Surgical surface anatomy and approach

The thyroid gland straddles the trachea anteriorly. It consists of two conically shaped lobes that are connected to each other by a narrow bridge, or isthmus, which may also have an ascending pyramidal lobe. The thyroid normally extends from the level of the fifth cervical vertebra to the body of the first thoracic vertebra. A normal thyroid gland weighs approximately 25 g in an adult, and each lobe on average measures 5 cm in length, 3 cm in width and 2 cm in thickness. The isthmus measures approximately 1.3 cm in length and usually overlies the second and third tracheal cartilages. Critical palpable surface landmarks for thyroid/parathyroid operations include the suprasternal notch, the cricoid cartilage, the thyroid notch and the hyoid bone. Normal anatomical surface landmarks may be significantly distorted or even lost because of enlargement of the thyroid itself or because of the patient's body habitus. In obese, ‘short-necked’ older patients, the thyroid tends to be positioned lower in the neck and may be almost entirely retrosternal ( Fig. 18.4 ). An enlarged thyroid gland may extend inferiorly into the mediastinum or superiorly into the submandibular region, and may even encroach on the lateral neck compartments and displace the carotid arteries and the internal jugular veins ( Fig. 18.5 ).

The patient undergoing a thyroidectomy/parathyroidectomy is usually positioned in some degree of neck extension in order to displace the thyroid anteriorly and superiorly. The precise location of the neck incision is important, and optimal placement requires consideration of both patient cosmesis and surgical access. Ideally, a gently curving, symmetrical, transverse incision that is placed along the skin lines of Langer, travelling either through or parallel to a neck crease, is preferred. As natural creases may be lost with extension, it is helpful to mark out the incision while the patient is in a neutral sitting position, even prior to anaesthesia. Traditional teaching has classically described placement of the thyroidectomy/parathyroidectomy incision ‘two fingers’ breadths above the suprasternal notch’. However, for individuals with long necks, such incisions are often too low and may hamper exposure of the superior pole. Conversely, for individuals with short necks, such incisions may be too high and limit access to their inferior pole, especially if a substernal goitre is present (see Fig. 18.4 ). Placement of the incision 1–2 cm below the cricoid cartilage, a landmark that consistently correlates with the location of the thyroid isthmus, will facilitate exposure and permit access to both superior and inferior thyroid poles. Exposure of the thyroid/parathyroid may be challenging in patients who are obese, or who have short necks or limited extension due to kyphoscoliotic deformities or other neck pathology, especially when in a position of fixed flexion. The actual length of the thyroidectomy incision really must be tailored to both the individual patient and their clinical presentation. During thyroidectomy/parathyroidectomy, the adequacy of surgical exposure of critical structures, including the RLNs and parathyroid glands, must not be compromised for incisional cosmesis.

Platysma lies beneath the skin and subcutaneous fat, and is often deficient in the midline ( Ch. 15 ). The working space for thyroidectomy is usually created by raising flaps along the subplatysmal plane, super­iorly to the level of the top of the thyroid notch, and inferiorly to the level of the suprasternal notch. When creating these flaps, care must be taken to avoid the bleeding that may occur as a result of injury to the anterior jugular veins or one of their tributaries. The anterior jugular veins run along the surface of the infrahyoid strap muscles, often paralleling the midline, but have a somewhat variable course. They also may communicate with each other through bridging vessels that cross the midline, especially lower in the neck. The anterior jugular veins usually empty into the internal jugular veins, but may also empty directly into the subclavian veins. The strap muscles are encountered beneath the platysma. They are paired muscles encased by the superficial layer of the deep cervical fascia and either originate or insert on to the hyoid bone; they function either to depress or to stabilize the hyoid bone during deglutition, and to stabilize the larynx. Individual strap muscles are each named according to site of origin and insertion. The inner strap muscles are the thyrohyoid more superiorly, and the sterno­thyroid more inferiorly. The thyrohyoid originates from the lamina of the thyroid cartilage above the insertion of sternothyroid (oblique line) and inserts on to the lower border of the greater cornu of the hyoid bone. The outer strap muscles are sternohyoid and omohyoid. Sternohyoid originates from the posterior aspect of the manubrium, the adjacent clavicle and the posterior sternoclavicular ligament, and inserts on the medial aspect of the lower border of the body of the hyoid bone. The omohyoid has an inferior belly that originates from the upper border of the scapula and the superior transverse scapular ligament, a central tendon enclosed by a band of cervical fascia that crosses the carotid sheath, and attaches to the clavicle and the first rib, and a superior belly that extends alongside sternohyoid to insert on the lateral aspect of the hyoid bone ( Ch. 15 ). All the strap muscles, except thyrohyoid, are innervated by the ansa cervicalis, derived from the cervical plexus (C1, C2, C3); thyrohyoid is innervated by fibres from C1 that travel with the hypoglossal nerve. The superior root of the ansa cervicalis appears as a branch of the hypoglossal nerve and descends along the lateral border of sternothyroid, innervating that muscle near its lower third. If the strap muscles must be transected during thyroidectomy to facilitate surgical exposure of a large goitre, this should be carried out at the level of the cricoid cartilage or higher up in order to preserve the nerve supply to the muscles. Occasionally, for suspected or known thyroid cancers that are located anteriorly within the gland and may invade the overlying strap muscles, leaving an island of muscle in continuity with the tumour as part of the surgical specimen may facilitate clearance at its anterior margin. Division of sternothyroid at its insertion is a manœuvre that may facilitate exposure of the superior pole of the thyroid. During thyroidectomy, the strap muscles are separated along their midline fascia; care must be taken when operating for suspected or confirmed thyroid malignancy because there may be pretracheal and prelaryngeal lymph node meta­stases present that should also be removed.

The thyroid gland is enveloped by an outer false capsule and an inner true capsule. The false capsule (surgical capsule, perithyroidal sheath) is continuous with the deep (pretracheal) layer of the middle or visceral layer of the deep cervical fascia. It is well developed anteriorly and laterally but thin posteriorly, although it thickens medially into the posterior suspensory ligament of the thyroid, commonly referred to as the ligament of Berry (LB). The LB suspends each thyroid lobe from the cricoid cartilage and the first two tracheal rings, and extends along the posteromedial aspect of each lobe. The true capsule sends septa into the gland parenchyma and forms lobules.

The superior parathyroid glands are usually located between the true and false thyroid capsules. The inferior parathyroid glands may be located intrathyroidally, or between the true and false capsules, or on the outer surface of the false capsule. During thyroidectomy, the false capsule may be appreciated as being in continuity with the areolar tissue that is bluntly pushed off the true capsule towards the paratracheal region when entering the central neck compartment. This manœuvre usually also mobilizes the parathyroid glands off, and away from, the thyroid. The importance of this capsular dissection technique, begun high on the surface of the true thyroid capsule and carried out in a medial to lateral direction, cannot be overstated because it facilitates preservation of the parathyroid glands by leaving their blood supply intact. When dissection is being performed within this plane, small terminal branches of the inferior thyroid artery that directly penetrate the surface of the thyroid gland are encountered and require careful systematic ligation or clipping in order to avoid haemorrhage ( Fig. 18.6 ).

The parathyroid glands may be differentiated from yellowish fat, dark brownish thyroid tissue and greyish to pinkish lymph nodes, on the basis of their pale tan to dark reddish brown colour; their appearance, with magnification, of being peppered with light-refracting pinpoint specks; and their characteristic flattened oblong shape with discrete rolled edges. Normal parathyroid glands weigh between 15 mg and 40 mg, measure approximately 2 mm × 3 mm × 5 mm, and are often enclosed by a small amount of fat. In 80% of cases, the superior parathyroid glands are located on the posterior aspect of the thyroid at the level of the cricothyroid junction, corresponding to a position that is 1 cm superior to the point where the RLN crosses the inferior thyroid artery. The inferior parathyroid glands are more variable in their position, and in 50% of cases may be found within 1 cm of the inferior thyroid pole, located either inferiorly, laterally or posteriorly. The superior parathyroid glands tend to be located lateral to the RLN sagittal plane and posterior (dorsal) to the RLN coronal plane, whereas the inferior parathyroid glands tend to be located medial to the RLN sagittal plane and anterior (ventral) to the RLN coronal plane ( Fig. 18.7 ). During subtotal parathyroidectomy carried out for the treatment of multigland disease (which has an inherent associated risk of disease recurrence and need for reoperation), the inferior parathyroid glands are given preference over the superior parathyroid glands as the source of the remnant that remains in situ , on the grounds that removing disease recurrence anterior to the plane of the RLN may have a lower risk of nerve injury during reoperative parathyroidectomy. Tagging of the parathyroid remnant with coloured suture or clips may also be helpful if disease recurrence requires reoperation. However, the most important consideration is to ensure that the parathyroid remnant left in situ has an adequate blood supply. Similarly, in order to minimize the risk of the patient developing postoperative hypoparathyroidism, preservation of the blood supply of all of the parathyroid glands left in situ is absolutely critical during thyroid/parathyroid operations. Each parathyroid gland should be coveted and treated as if it is the only remaining parathyroid. Great care must be taken to preserve the branches of the inferior thyroid artery that supplies both the upper and lower parathyroid glands, and the superior thyroid artery that often also supplies the superior parathyroid glands.

Intensive scrutiny of the viability of the parathyroids is important; devitalization should not be confused with the bruising or colour change that is observed due to development of a subcapsular haematoma. In circumstances where a normal parathyroid gland is intentionally or inadvertently removed or devitalized, parathyroid autotransplantation should be carried out. After intraoperative confirmation that the removed or devitalized tissue is indeed parathyroid, using either frozen section analysis or another technique, autotransplantation may proceed. The parathyroid tissue is initially placed in ice-cold saline while the autotransplantation implantation sites are prepared. Even though many different anatomical sites for parathyroid autotransplantation have been described, they may broadly be classified as being either subcutaneous or intramuscular. If the tissue to be autotransplanted is derived from a grossly normal-appearing parathyroid gland, removed during a thyroid operation from a patient with normal parathyroid function, immediate autotransplantation should be performed. In this setting, the sternocleidomastoid is an easily accessible, well-vascularized and commonly utilized autotransplant implantation site. However, if the parathyroid tissue being autotransplanted originates from a hyperparathyroid patient and/or appears grossly abnormal, if autotransplantation is warranted, a more distant host site, such as brachioradialis, should be selected. Should recurrent hyperparathyroidism develop in such a patient, preoperative localization and surgical re-exploration may be more straightforward, and have less associated morbidity, in a location that is remote from the neck. In renal failure patients, avoiding potential or existing arteriovenous fistula sites is an important consideration when selecting an autotransplant implantation site. Several tiny pockets are created within the host muscle to receive aliquots of the parathyroid tissue that has been diced into approximately 1 mm ² fragments. It is critically important for there to be no bleeding within the muscle pockets because bleeding and clot may prevent parathyroid tissue engraftment. The implantation sites are also each marked with clips or non-absorbable suture ( Fig. 18.8 ). Injection of morcellated parathyroid tissue suspended in saline into the muscle is an alternative autotransplantation technique. If excessive parathyroid tissue is available, as is often the case in secondary or tertiary hyperparathyroid patients, parathyroid cryopreservation should be considered.

Due to goitrous enlargement, the lower pole of the thyroid may extend into the anterior superior mediastinum and cause tracheal compression at the thoracic inlet within the rigid space created by the surrounding bony structures ( Fig. 18.9 ). The patient may be symptomatic as a consequence of significant segmental tracheal and oesophageal compression. However, the majority of such goitres may be removed through a standard transcervical approach, and usually just requires blind blunt finger dissection to allow for delivery of the substernal component out of the chest and into the neck ( Fig. 18.10 ). In such cases, the RLN may be at increased risk of injury, especially if it is adherent or splayed by the goitre, and not identifiable until the goitre has been delivered from the chest. Other techniques for delivery of a substernal goitre include the drawer manœuvre, where the surgeon grasps the goitre from the neck with two hands and pulls it out like a drawer; and morcellation, which may be hazardous because it can lead to haemorrhage, dissemination of malignancy and retention of a substernal remnant. A partial sternotomy may be required for rare cases. Dumbbell-shaped goitres and reoperative substernal goitres are both at higher risk of requiring a sternotomy. Injury to the cupola of the pleura with a resultant pneumothorax is an uncommon complication that may occur during removal of a substernal goitre.

There has been widespread adoption of preoperative image-directed focused parathyroidectomy, usually carried out through a small incision, guided by intraoperative parathyroid hormone measurement, and performed as a same-day hospital discharge procedure for treatment of primary hyperparathyroidism. However, all surgeons who perform these focused procedures must also be able to perform a four-parathyroid gland exploration readily, should it become necessary when multiple abnormal parathyroid glands are identified. A four parathyroid gland exploration is also required for focused parathyroidectomy cases in which preoperative imaging studies fail to localize, misdirect or are incorrect, for treatment of secondary or tertiary hyperparathyroidism, lithium-related hyperparathyroidism and hereditary forms of hyperparathyroidism.

The major operative objective when performing a parathyroidectomy for the treatment of primary hyperparathyroidism is the identification and removal of one or more abnormal glands that are causing the disease. The objective when performing a subtotal parathyroidectomy for treatment of four-gland disease, whether for treatment of primary, secondary or tertiary hyperparathyroidism, is the removal of all parathyroid tissue except for one half of a normal gland, or leaving the patient with 50 mg of viable parathyroid tissue. Though often carried out through small incisions today, the initial exposure of the central neck for parathyroidectomy is essentially the same as for thyroidectomy, with medial retraction on the thyroid lobe permitting adequate central neck exposure. Intraoperatively, based on their gross appearance, both normal and pathological parathyroid glands may be identified. Intraoperative localization of abnormal parathyroid glands is greatly facilitated by preoperative imaging studies. The superior parathyroid glands are usually more consistent in location than the inferior glands, which are situated along the posterior surface of the superior pole of the thyroid gland, lateral to the RLN sagittal plane and posterior (dorsal) to the RLN coronal plane (see Fig. 18.7 ). The utility of the ZT in assisting with superior parathyroid gland localization has already been reviewed (see Fig. 18.3 ). The inferior parathyroid glands have a more variable position and generally are described as being medial to the RLN sagittal plane and anterior (ventral) to the RLN coronal plane (see Fig. 18.7 ). The RLN actually serves as a very useful anatomical landmark for correctly distinguishing between superior and inferior parathyroid glands.

Correct designation of a parathyroid gland as being either superior or inferior is important because it helps to direct the surgical exploration for glands that have not yet been identified ( Fig. 18.11 ). The inferior parathyroid glands may be located on the lateral, anterolateral or posterior aspect of the lower portion of the thyroid lobe, a short distance inferior to the lower pole of the thyroid, within the thyrothymic ligament, and may even be incorporated into the thymus. Multiple factors may contribute to difficulties with parathyroid gland identification during operation, including the limited experience of the surgeon, incorrect diagnosis, non-localized disease, patient characteristics (such as a short neck or obesity), normocalcaemic disease, the presence of a concurrent multinodular goitre or other thyroid pathology, central neck lymphadenopathy, and a history of a prior central neck compartment operation. Clear identification of the normal parathyroid glands is also often necessary to aid in deducing the side and type (superior versus inferior) of a missing gland, and may help to direct surgical exploration. Intensive scrutiny and comparison of the size and morphology of the normal parathyroid glands that have been identified during operation may allow for the diagnosis of what was not initially appreciated as being multigland disease. In this setting, intraoperative frozen section tissue analysis may be especially important for definitive parathyroid identification. The strategy for localization of a missing parathyroid gland may require exploration superior to the upper pole of the thyroid as high as the hyoid bone, and inferior to the lower pole of the thyroid into the superior mediastinum. The exploration begins with careful inspection and palpation of the posterior and lateral aspects of the thyroid capsule. Removal of paratracheal tissue and delivery of the thymus gland into the neck with gentle upward traction, along with careful division of its vessels as they are encountered, may also be necessary. Further careful systematic exploration of the parapharyngeal and retropharyngeal spaces, and the para-oesophageal and retro-oesophageal spaces should follow. This exploration is carried out deep within the paratracheal space both anterior and posterior to the plane of the RLN. The missing parathyroid may even be located immediately anterior to the point at which the RLN enters the larynx. If the parathyroid continues to elude the surgeon, then opening the carotid sheath and exposing the common carotid artery for its course in the neck may expose the ectopic gland. When all sites have been explored, then either ligation of the inferior thyroid artery or thyroid lobectomy may be performed in order to devitalize or remove what may be an ectopic intrathyroidal gland. Sternotomy for mediastinal exploration should not usually be carried out at the initial operation if a missing parathyroid(s) has not been identified, but should be deferred until the diagnosis has been reconfirmed and further localization studies have been performed.

Surgical anatomy and variants