Thyroid cancer is the most common malignant tumor of the endocrine system (90%). The incidence of thyroid cancer has been on the rise worldwide in recent years, especially in coastal areas of China. Since thyroid cancer is often associated with lymph node metastasis in the neck, neck debulking is an important part of thyroid cancer treatment. With the continuous evolution of neck clearance from emphasizing radical treatment over function to both radical treatment and function, and then to both radical treatment, function and appearance, elective neck clearance with low collar incision to preserve the cervical plexus began to be gradually used in the treatment of differentiated thyroid cancer.
Cervical clearance has been available for a century. Crile in Cleveland, USA, inspired by Halsted axillary lymph node dissection, started to apply regional lymph node dissection to the neck and reported 132 cases of cervical lymph node dissection in the Journal of the American Medical Association in 1906 for the first time [1]. After the 1960s, with the formation and development of multidisciplinary integrated treatment such as surgery, radiotherapy and chemotherapy, modified cervical dissection began to be promoted in the clinic, which is based on the preservation of the paraspinal nerve and can be performed simultaneously with the preservation of the internal jugular vein and/or the sternocleidomastoid muscle [2]. In 1991, the American Academy of Otolaryngology-Head and Neck Surgery Foundation divided neck clearance into four categories according to the scope of surgical clearance: (1) classical neck clearance; (2) modified neck clearance; (3) elective neck clearance (including suprascapularis lingualis clearance, lateral neck clearance, posterior lateral neck clearance, and anterior neck clearance). In 2001, the American Academy of Head and Neck Surgery and the American Academy of Otolaryngology-Head and Neck Surgery Foundation further modified the above classification by declassifying the elective cervical dissection and only recommending the specific subdivisions (zones I-VII) to be dissected.
Most of the metastatic lymph nodes in the neck are located between the superficial and deep fascia of the deep cervical fascia. The deep cervical fascia wraps around the muscles, nerves, blood vessels and lymphatic tissues respectively, isolating them from each other and acting as a certain barrier. In 1967, Bocca et al. summarized the supraglottic laryngeal carcinoma by proposing a modified neck clearance procedure that could preserve the important tissue structures of the neck, including non-lymphoid tissues such as the cervical plexus nerve [3]. in 1995, the Canadian Porter was the first to systematically describe cervical plexus-preserving neck clearance in the American Journal of Surgery in 1995 and confirmed the safety and efficacy of this procedure [4]. Because of the better prognosis of differentiated thyroid cancer, the metastatic lymph nodes are mostly free of extraperitoneal invasion; and the patients are mostly young and middle-aged with high functional and cosmetic requirements, elective neck dissection with collar incision to preserve the cervical plexus is being more and more widely used in differentiated thyroid cancer. In this paper, we retrospectively analyzed 112 cases of this procedure performed in our department from January 2009 to December 2010.
1 Clinical data
1.1 Study population From January 2009 to December 2010, a total of 112 first-time patients with thyroid cancer underwent elective neck clearance with a collar incision to preserve the cervical plexus, including 6 patients with bilateral clearance. Inclusion criteria: For first-time patients with differentiated thyroid cancer with clinically considered or puncture-confirmed metastasis in the lateral cervical region. Exclusion criteria: (1) lymph node metastasis in area VA; (2) metastatic lymph nodes >3 cm in diameter; (3) obvious fusion, extravasation or fixation of lymph nodes; (4) history of non-standard neck clearance or deep surface lymph node biopsy of sternocleidomastoid muscle. Among them, 34 cases were male; 78 cases were female. The age ranged from 10 to 68 years old, with an average of 38 years old. Pathology showed papillary carcinoma in 111 cases and follicular carcinoma in 1 case.
1.2 Surgical methods and techniques
A low collar incision was made about one transverse finger from the clavicle, externally to the posterior border of the affected sternocleidomastoid muscle and internally to the anterior border of the healthy sternocleidomastoid muscle. The skin and broad cervical muscle are incised, and the skin is freed anteriorly to the midline of the neck, posteriorly to the external jugular vein, inferiorly to the supraclavicular, and superiorly to the submandibular gland, avoiding excessive upward freeing to damage the mandibular border branch of the facial nerve. Separate the fascia of this muscle along the anterior border of the sternocleidomastoid muscle, up to the inferior border of the parotid gland, taking care to protect the superior segment of the external jugular vein and the greater auricular nerve, and down to the superior sternal recess. Pull up the sternocleidomastoid muscle and free its posterior fascia to the posterior edge of the muscle, protecting the inferior segment of the external jugular vein below the posterior aspect of the muscle, paying attention to ligating its nutrient vessels, which are one of the common causes of postoperative bleeding.
The submandibular gland was opened and pulled upward to reveal the posterior belly of the diastasis muscle below it, and the lymph nodes in area IIA were cleared from the inside out. The internal jugular vein and its branches are exposed along the inferior border of the bicipital muscle, and the tissue behind the superior sternocleidomastoid muscle, below the posterior ventral part of the bicipital muscle and lateral to the internal jugular vein is separated, and the paraspinal nerve is free and pulled posteriorly and superiorly to clear the lymph nodes in zone IIB. The lymph nodes in area IIB are difficult to be cleared. Attention should be paid to: (1) there are often small arteries passing between the deep posterior ventral surface of the bicipital muscle and the internal jugular vein and the paraspinal nerve, which should be ligated to avoid uncontrollable bleeding; (2) when the hypoglossal nerve is in a low position below the posterior ventral surface of the bicipital muscle, attention should be paid to avoid accidental injury; (3) some of the cervical plexus has traffic branches that converge into the paraspinal nerve in area II, which should be preserved to protect the functional integrity of the paraspinal nerve. (3) Some of the cervical plexus has traffic branches that converge into the paraspinal nerve in zone II, so care should be taken to preserve the functional integrity of the paraspinal nerve.
The scaphoid hyoid muscle is preserved (or tied off), the carotid sheath is opened, the common carotid artery and vagus nerve are dissociated, the specimen is turned outward to the lateral aspect of the internal jugular vein, the internal jugular vein is pulled inward, the prevertebral fascia is exposed, and the cervical Ⅱ, Ⅲ, and Ⅳ nerve roots are exposed, and the lymph nodes in the Ⅲ and Ⅳ regions are cleared in the order from the inside up to the outside down, which can effectively protect the cervical Ⅱ, Ⅲ, and Ⅳ nerves. Pay attention to clearing the lymph nodes between the nerve roots and their posterior area to avoid omission; also pay attention to protecting the nerve root trophic vessels to avoid postoperative bleeding. In some patients, the external jugular vein may have variation and converge directly into the internal jugular vein at the location of zone III, which should be protected with care.
When clearing the lymph nodes in zone IV and zone VB downward, reveal and protect the transverse cervical artery and its deep phrenic nerve, pay attention to ligating the branches of the transverse cervical artery, and clear the lymph nodes in the supraclavicular region along the clavicle. When clearing the internal jugular vein angle area, attention was paid to ligating the thoracic duct or the right lymphatic duct. Due to the anatomical relationship, there were significantly more celiac leaks on the left side than on the right side. There are more variations in the anatomy of the thoracic duct: (1) into multiple thoracic ducts converging into the internal jugular vein angle or subclavian vein; (2) the location of the convergence is located at the end of the internal jugular vein, external jugular vein or complex multi-pathway reflux; (3) the end of the thoracic duct forms a lymphatic plexus, often with multiple branches. The lymphatic duct wall is thin, the tissue is brittle, and the resistance to traction is weak, so it is easy to tear during operation. It is not necessary to deliberately search for lymphatic ducts when clearing this area, but should be carefully separated, ligated gently, and avoided traction. The lymphatic adipose tissue between the sternocleidomastoid head and the clavicular head should be cleared, and the lymphatic adipose tissue can be cleared from inside to outside along the surface of the anterior jugular arch to ensure the thoroughness of the operation.
At the end of the cervical sweep, the affected thyroid lobe and isthmus were then excised, and the lymph nodes in the central region were cleared at the same time, including the cricothyroid lymph nodes, the tracheal and anterior thyroid lymph nodes, and the intertracheoesophageal lymph nodes, and part of the upper pole of the thymus was excised, and its deep surface lymph nodes were also cleared.
2 Results
2.1 A total of 118 elective neck dissection with low collar preservation of the cervical plexus was performed in 112 patients, and the metastatic lymph nodes were mainly distributed in zone VI (78.8%), zone IV (72.9%), zone III (60.2%), zone II (43.8%) and zone VB (16.9%).
2.2 Two cases of postoperative complications of bleeding: one case of bleeding from the trophic branch of the sternocleidomastoid muscle and the other case of bleeding from the branch of the transverse carotid artery were treated with emergency debridement and hemostasis; three cases of complications of celiac leakage were treated conservatively with strong negative pressure suction and external pressure on the angle of the internal jugular vein, which healed 3-7 days after surgery.
2.3 Sensory measurement was performed by light touch or pinprick compared with the healthy side of the neck, and none of the patients had any significant postoperative sensory abnormalities in the ear, lower neck and shoulder.
2.4 There was no recurrence in the lateral cervical region after the operation by 1 to 25 months follow-up.
3 Discussion
The scope and indications for elective lymph node dissection in the lateral cervical region of differentiated thyroid cancer have been controversial for a long time, especially the selection of the area to be dissected. Papillary carcinoma is the most common and the pathological type of thyroid cancer with a high rate of lymph node metastasis, with a rate of 30-90% in the cervical lymph nodes [5]. Although lymph node metastasis does not affect the overall survival rate of papillary thyroid cancer, it increases the recurrence rate in localized areas of the neck.
3.1 Rationalization of the surgical approach
The literature reports that the main areas of lymph node metastasis in the lateral neck region of papillary thyroid carcinoma are zones III, IIA, and IV. Lee et al. confirmed by examining 167 papillary thyroid carcinoma specimens with lymph node metastasis in the neck that the most common sites of metastasis in the lateral neck region were zones III (80.6%), IV (74.9%), and II (55.5%), respectively [6]. Similar to the present study, Frankenthaler confirmed that the most frequent areas of lymphatic metastasis in differentiated thyroid cancer were zones VI (90%), IV (52%) and III (45%), followed by zones VB (33%) and IIA (30%); while no metastases were seen in zones I, IIB and VA [7].
The main controversy regarding lateral cervical zone clearance with preservation of the cervical plexus has focused on the need for routine clearance of zone IIB. Zone IIB is defined as the area of tissue located below the plane of the paraspinal nerve, deep to the fascia of the cephalic and scapularis raphe muscles, superiorly and laterally to the caudalis lingualis muscle, posteriorly to the sternocleidomastoid muscle, and superiorly to the skull base [8]. In Lee’s study, lymph node metastasis rates of 55.5% and 6.8% were found in regions IIA and IIB, respectively, while patients with metastasis in region IIB were accompanied by metastasis in IIA. It is proposed that routine clearance of zone IIB is not necessary in cases where metastases are relatively limited or where there are no clear metastases in zone IIA [6]. This conclusion was supported by Farrag, in which the lymph node metastasis rate was 60% in 59 cases of routine zone II debulking, of which only 8.5% were in zone IIB, and all metastases in zone IIB were accompanied by metastases in zone IIA [9]. Combined with the above studies, in the lateral cervical zone clearance, this zone must be cleared if clinical or imaging suggests metastasis in zone IIB; when the preoperative clinical assessment of zone IIA is negative, when puncture cytology is not confirmed or when no metastasis is considered intraoperatively, whether routine clearance of zone IIB is still required remains to be further investigated.
The extent of zone V clearance is another controversial point for lateral cervical zone clearance with preservation of the cervical plexus. Zone V is the triangular area between the posterior border of the sternocleidomastoid muscle, the anterior border of the trapezius muscle and the supraclavicular area, which can be subdivided into zone VA (paracervical chain lymph nodes) and zone VB (paracervical and supraclavicular lymph nodes) [9]. Given the relatively low rate of lymph node metastasis in zone V, Caron suggested that zone V may not be routinely cleared unless metastasis in this zone is considered clinically or on imaging [10]. However, in Farrag’s study, it was found that in N1b+ patients, although no metastasis was found in zone VA, the rate of lymph node metastasis in zone VB was 40%, a finding consistent with Frankenthaler’s study [7,9]. In our study, the rate of lymph node metastasis in area VB also reached 16.9%, suggesting the need for routine clearance of area VB for lateral cervical plexus preservation, even if metastasis in this area is not considered clinically or on imaging.
In combination with the present study, lateral neck clearance with preservation of the cervical plexus has covered the common metastatic areas (II, III, IV and VB) of differentiated thyroid cancer, suggesting that this procedure should be reasonable and safe for some selective N1b+ patients. Due to the lack of prospective studies and long-term follow-up data, whether this procedure increases the local recurrence rate remains to be confirmed by further studies.
3.2 Indications and contraindications for surgery
The indications for lateral cervical region clearance with preservation of the cervical plexus are inconclusive. The relative indications for surgery are: N1b+ differentiated thyroid cancer (except metastasis in VA) with small metastatic lymph nodes (≤3 cm in diameter) and no extraperitoneal invasion. Relative contraindications to surgery are (1) those with a history of irregular neck clearance or deep sternocleidomastoid muscle lymph node biopsy before surgery; (2) those with extensive cervical lymph node metastasis or significant lymph node extravasation [11,12].
3.3 Postoperative complications and management
3.3.1 Postoperative bleeding is the most common postoperative complication, including bleeding from the trophic vessels of the cervical nerve root, the trophic branches of the medial surface of the sternocleidomastoid muscle, the branches or ruptures of the internal jugular vein, subcutaneous bleeding and bleeding from the branches of the transverse cervical artery. It is often caused by coughing, vomiting or moving of the patient after awakening from anesthesia and other triggers that make the threads of the ligated vessels fall off or the electrocoagulated vessels reopen. Compressing the neck wound during anesthesia extraction can effectively reduce the occurrence of postoperative bleeding. If postoperative swelling of the incision, purple local skin, high drainage and clots are found, it is mostly active bleeding and should be cleared to stop bleeding in time.
3.3.2 Celiac leakage is not uncommon. When clearing the internal jugular vein angle, gentle operation, careful ligation and routine local coverage with gelatin sponge can effectively reduce the occurrence of postoperative celiac leakage. Once celiac leakage occurs, strong negative pressure suction of the neck (60~80KPa) or external pressure in the area of the internal jugular vein angle should be promptly applied. If the drainage fluid does not decrease but increases after conservative measures, reaching more than 600~800 ml per day, the thoracic duct or the main trunk of the right lymphatic duct should be considered to be damaged and should be promptly surgically explored and ligated.
3.3.3 Postoperative upper neck swelling is more common, and the local skin may show inflammatory manifestations. Under the exclusion of local bruising, it may be related to intraoperative over-drawing of the sternocleidomastoid muscle causing blunt injury, injurious lymphedema, celiac leakage or infection, etc. The effect of topical application of local Jinhuang San is good.
3.3.4 Postoperative lymph node enlargement in area VA Some patients may have lymph node enlargement in area VA during postoperative follow-up, which may be related to poor local lymphatic drainage, and the puncture is often lymphadenitis or lymph node reactive hyperplasia, which does not require treatment and regular follow-up.
3.4 Advantages and disadvantages of the procedure
The elective zone clearance with preservation of the cervical plexus preserves the supraclavicular nerve, the lesser occipital nerve and the greater auricular nerve of the cervical plexus under the premise of ensuring radical treatment, which can significantly improve the postoperative sensory abnormalities of the lower neck, shoulder and peri-auricular skin of the patient. Although the transverse cervical cutaneous nerve will inevitably be cut during the separation of the anterior border of the sternocleidomastoid muscle, the contralateral cervical plexus traffic branch can compensate for the sensory deficit in the anterior cervical region. The cervical lymph node metastasis of head and neck malignant tumors usually does not involve the lymph nodes around the external jugular vein, and preserving the external jugular vein does not affect the thoroughness of surgery, which can significantly improve the blood return to the face and reduce postoperative facial tissue edema. The confluence of the cervical plexus traffic branch is an important part of the paraspinal nerve fibers, which may have a certain innervating effect on the sternocleidomastoid muscle, especially the trapezius muscle, so it should be protected as much as possible during neck clearance, which can effectively avoid the occurrence of shoulder-arm-syndrome (shoulder-arm-syndrome) in patients after surgery. Differentiated thyroid cancer is commonly seen in young and middle-aged women and requires a high level of appearance of the neck incision. Therefore, a low collar incision is adopted in the neck clearance surgery to make the incision line coincide with the skin pattern of the neck, which ensures the maximum preservation of neck function and appearance on the premise of radical treatment and improves the quality of life of patients, which is in line with the modern tumor treatment concept. The main drawback of this procedure is that the incision line can be closed to the skin line of the neck.
The main disadvantage of this procedure is that it is relatively difficult to reveal zone II. The operator should be familiar with the neck anatomy and have the foundation of skilled neck clearance technique. It must be repeatedly emphasized that when the cervical lymph node metastasis is extensive or the lymph nodes have obvious invasion or fixation, a longitudinal incision or a classical or modified cervical dissection should be added according to the specific situation to ensure the thoroughness of the operation.