Current Opinion in Oncology:
ENDOCRINE TUMORS: Edited by Julie Ann Sosa
Surgical management of the lateral neck compartment for metastatic thyroid cancer
Dralle, Henning; Machens, Andreas
Department of Surgery, University Hospital, Medical Faculty, University of Halle-Wittenberg, Halle, Germany
Correspondence to Henning Dralle, MD, FRCS, FACS, Professor of Surgery and Chairman, Department of General, Visceral and Vascular Surgery, University Hospital, Medical Faculty, University of Halle-Wittenberg, Ernst-Grube-Str. 40, D-06097 Halle/Saale, Germany. Tel: +49 345 557 2314; fax: +49 345 557 2551; e-mail: firstname.lastname@example.org
Purpose of review: The lateral neck compartment is the second most frequent target region for metastatic papillary thyroid cancer (PTC) and medullary thyroid cancer (MTC). Lateral lymph node metastases are associated with locoregional recurrence and, when they involve either side of the neck, with mediastinal and distant metastases.
Recent findings: For tumors originating from the upper thyroid pole, the first nodal basin is not invariably the central compartment (as for primaries arising from the inferior thyroid pole) but often the upper part of the ipsilateral lateral compartment. Lymph node dissection of the first basin may differ depending on the location of the primary tumor. Involvement of the contralateral lateral compartment is seen in PTC with extensive central compartment involvement, and in MTC with preoperative basal calcitonin levels more than 200 pg/ml (normal limit <10 pg/ml).
Summary: After lateral lymph node dissection for metastatic thyroid cancer, dysfunction of lateral neck nerves is fairly common. This observation underpins the importance of striking a balance between oncological benefit and surgical risk. Lateral lymph node dissection may be warranted for an upper thyroid pole primary, for a tumor with extensive involvement of the central compartment, and for an MTC with increased basal calcitonin level of 20–200 pg/ml (ipsilateral dissection) or more than 200 pg/ml (bilateral dissection).
The lymphatic system, positioned centrally in the neck, carries the lymph away from the thyroid gland in a centrifugal direction. As a result, locoregional spread of thyroid cancer predominantly involves the ipsilateral, and sometimes also the contralateral central and lateral neck nodes [1–4]. Involvement of the contralateral lateral lymph node metastases is associated with an increased risk for mediastinal and distant metastases [3,5,6].
Ipsilateral neck metastases represent the first basin of lymphatic tumor cell dissemination, which is modulated by the anatomical location of the primary thyroid tumor. Papillary thyroid cancers lodging in the upper thyroid pole often spread first to the upper parts of the ipsilateral lateral compartment, whereas primary tumors arising from the mid and lower portions of the thyroid gland favor the central compartment [7▪,8▪▪]. The different drainage of the superior and inferior thyroid pole is a natural consequence of the peculiar anatomy of the thyroid gland's lymphatic system, which is organized in parallel to the gland's venous drainage system: lymph vessels draining the upper thyroid pole accompany the superior venous vessels to the ipsilateral lateral neck nodes; lymph vessels draining the middle portion of the thyroid gland follow the middle venous vessels to the middle internal jugular nodes; and lymph vessels draining the inferior thyroid pole course together with the inferior pole veins to the central and lower ipsilateral lateral (supraclavicular) nodes [9,10] (Fig. 1). From an oncologic point of view, the ipsilateral and contralateral lateral neck may be conceived as a therapeutic watershed: lymph node metastasis to the ipsilateral lateral compartment usually reflects localized disease that is curable through systematic lymph node dissection, whereas involvement of the contralateral lateral compartment heralds advanced, most often systemic disease.
Because of the surgical ramifications of unilateral as opposed to bilateral involvement of the lateral neck, preoperative imaging plays a key role in clarifying the need for, the extent, and the nature (’curative’ versus ‘palliative’) of lateral neck surgery in the absence or presence of distant metastases. The higher is the index of suspicion for distant metastases, the more carefully lateral neck surgery must balance the oncologic benefit deriving from the procedure with the attendant surgical morbidity [11,12]. Although the surgical complications of central compartment dissection [13–18] are well characterized, the surgical morbidity resulting from lateral compartment dissection has rarely been analyzed in a systematic fashion [19,20]. Because of the renewed interest in lateral compartment surgery worldwide , it may be pertinent to review recent trends of surgical indications for lateral neck dissection in patients with papillary thyroid cancer (PTC) and medullary thyroid cancer (MTC). Important risk factors of surgical complications will be described that must be factored into treatment plans to dissect, or not dissect, the lateral neck compartment, and if so, the extent of that dissection. Exempt from this review are follicular and undifferentiated thyroid cancers, for which lymph node dissections are mostly palliative.
LATERAL NECK DISSECTION FOR PAPILLARY THYROID CANCER
Careful analysis of the histopathological pattern of central and lateral lymph node metastases in PTC uncovered two avenues of lymphatic tumor cell dissemination to the ipsilateral neck:
1. Direct spread from a primary tumor positioned in the upper thyroid pole to the upper part of the ipsilateral lateral neck compartment [7▪]. In those 20% of patients with PTC and no involvement of the central neck compartment [1,7▪,8▪▪,22], the ipsilateral lateral compartment is the first basin of lymphatic spread.
2. Involvement of the lateral in conjunction with the central neck compartment, which is the usual scenario for the presentation of lateral lymph node metastases . The causative primary is typically located in the middle and lower portions of the thyroid gland [8▪▪]. When more than five lymph node metastases are involved in the central neck, the ipsilateral lateral neck compartment is also involved . Conceptually, lymphatic tumor cell dissemination may progress via the posterior central lymph nodes in the paraesophageal area of level VII to the ipsilateral lateral neck nodes , or alternatively through direct lymphatic channels to the lateral jugular chain, as seen in upper thyroid pole primaries.
All in all, contralateral are less common than ipsilateral lymph node metastases [23,25–27]. Recognized risk factors for contralateral involvement include a larger number of central lymph node metastases  and advanced tumor stage.
Preoperative imaging, typically high-resolution ultrasonography with or without fine needle aspiration cytology and determination of thyroglobulin concentrations in the washout, takes center stage in deciding on the surgical strategy for metastatic PTC [28–31]. Although unilateral and bilateral therapeutic lateral neck dissection with curative intent is widely recognized, prophylactic lateral neck dissection is controversial. To clear those occult lymph node metastases that are found in 15% of ultrasonography-negative patients , some practice guidelines advocate prophylactic lateral node dissection, whereas others do not for lack of evidence that prophylactic lymph node dissection improves cause-specific survival .
In light of these data, prophylactic lateral neck dissection is warranted for locoregional control in patients with clinically node-negative PTC when one or more of the following conditions are present (Table 1):
1. Ipsilateral lateral dissection: if the primary tumor is located in the upper thyroid pole, and/or there is evidence of extensive involvement of the ipsilateral central compartment;
2. Bilateral lateral dissection: upon evidence of extensive involvement of the bilateral central compartment.
More research is needed to clarify whether the presence of multifocality, adverse histopathology, and advanced tumor stage warrants prophylactic lateral neck dissection.
LATERAL NECK DISSECTION FOR MEDULLARY THYROID CANCER
Like PTC, MTC has a propensity for early invasion of lymphatic vessels but does not concentrate radioiodine and differs from PTC in many other ways:
1. Distant metastasis occurs earlier in MTC than PTC, beginning at a primary tumor diameter of 1 (MTC) as opposed to 2 cm (PTC), and is twice as common [33,34]. It correlates positively with the number of lymph node metastases (1–10; 11–20; and >20 nodes), which reflects the disease burden [35▪▪] and survival . Biochemical cure is unlikely to be attained when 10 or more lymph nodes are involved . All in all, MTC is much more a systemic disease than PTC.
2. Intriguingly, stromal desmoplasia on thyroid histopathology may indicate the absence of lymph node metastasis in MTC. In 186 patients with MTC, the presence of stromal desmoplasia always signaled the absence of lymph node metastases [38–40]. If this finding is confirmed, patients with stromal desmoplasia on frozen section may no longer need lymph node dissection concomitant with thyroidectomy. Because information on biochemical cure and the number of removed nodes was not specified, this observation is awaiting validation in independent series.
Although preoperative ultrasonography has limited value for prediction of surgical cure or detection of metastatic nodes [41–43], many practice guidelines, including the American Thyroid Association (ATA) management guidelines , rely on this imaging modality to determine the need for ipsilateral or bilateral lateral dissection. To make this determination, preoperative basal calcitonin serum levels [45▪▪] may be more useful than preoperative ultrasonography or the number of central lymph node metastases . In 268 previously untreated patients with MTC, the ipsilateral and contralateral lateral neck was involved when basal calcitonin levels ranged between 20 and 200 pg/ml (normal limit <5–10 pg/ml) [45▪▪]. These data suggested that a central and ipsilateral lateral neck dissection may be adequate for patients with preoperative basal calcitonin levels of 200 pg/ml or less, whereas it may be prudent to consider a central and bilateral lateral neck dissection after that threshold has been crossed.
Controversy continues to surround the extent (unilateral versus bilateral) of lateral neck dissection for a disease that is frequently systemic at the time of presentation, enabling biochemical cure in no more than 60% of patients with node-negative and 10–20% of patients with node-positive MTC [3,34]. These issues are best addressed during the informed consent process, striking a balance between oncological benefit, surgical morbidity, and the inconvenience and costs of follow-up for persistent disease.
EXTENT OF LATERAL NECK DISSECTION
Several classification systems, delineating the anatomical borders of the central, lateral, and mediastinal compartments with the respective nodal groups, have been put forward [46–51], all of which have inherent strengths and weaknesses. Remarkably, all classification systems consistently define the common carotid artery as the landmark delimiting the lateral from the central neck compartment. Likewise, the clavicles and the right and left subclavian veins mark off the lateral compartment inferiorly. On the contrary, the lateral compartment is ill-defined superiorly and laterally, reflecting the lack of suitable anatomical landmarks in the submandibular and nuchal area of the neck .
Selective (’berry picking’) as opposed to systematic neck dissection is associated with higher rates of locoregional recurrence  and has been largely abandoned. Currently, most lateral compartment dissections routinely encompass levels II–V . A few studies with long-term follow-up assessed the need for removal of the lateral compartment in part or as a whole. In a retrospective study with a 4.5-year follow-up, Orlo Clark's group reported that not all patients with PTC required dissection of level I and V, decreasing the overall surgical complication rate . No such study has appeared for MTC as of this writing. Conceivably, sentinel lymph node biopsy may help determine the need for, and the extent of, lateral compartment dissection, but this proposition has not been evaluated in studies of sufficient duration [55,56]. At the moment, dissection of the complete lateral compartment, comprising levels II–V, represents the gold standard of lateral neck dissection. Nevertheless, for PTC in particular, further research is needed to define precisely those variations in lymphatic tumor spread that may allow, without worsening oncological outcome, a reduction in the extent of lateral dissection and surgical complications.
SURGICAL MORBIDITY OF LATERAL NECK DISSECTION
Lateral compartment dissection is not associated with fewer early and late surgical complications than central compartment dissection. Although injury to the recurrent laryngeal nerve and the parathyroid glands has been researched extensively, only a few studies have specifically dealt with the surgical morbidity of lateral neck dissection.
Owing to numerous posterior collaterals, the clearance of lateral neck nodes does not impair the lymphatic drainage of the neck. Nonetheless, lateral compartment dissection may give rise to two key complications that occur early and late after the operation: lymphatic leakage, and spinal accessory nerve damage resulting in shoulder dysfunction, which may be painful. Although less common, the cervical plexus, the sympathetic trunk, and phrenic, hypoglossal, and vagal nerves can also become subject to injury, usually during resection of locoregional disease or during extensive neck dissection. No data are available from the literature regarding frequency and socioeconomic burden entailed by these nerve injuries. Intriguingly, lateral (phrenic) and central neck (recurrent laryngeal) nerve palsies may work in synergy, causing serious respiratory problems. Carotid artery rupture, although rare, is almost invariably fatal. This life-threatening complication represents the catastrophic climax of a deep-seated wound infection in connection with a skeletonized carotid artery or previous neck irradiation [57,58].
After thyroidectomy and lateral neck dissection, chyle leakage is observed in 0.5–8% of patients [20,59–61], usually near the junction of the left subclavian and left internal jugular veins . Lymphatic leakage predisposes to infection of the neck wound and prolongs hospitalization. In our experience, the intraoperative use of milk-based solutions is not always suited to pinpoint the lymphatic leak inside the operative field. More helpful is the meticulous dissection of the entry of the thoracic duct into the venous angle using magnifying glasses. Lymphatic leaks should be ligated upon detection, avoiding the use of suture ligations that can tear the delicate wall of the leaking lymph vessel. Lymphatic leaks tend to appear on the first or second postoperative day or may not manifest clinically before the seventh postoperative day . There is still some conflict of opinion on whether postoperative lymphatic leaks are to be closed surgically or treated conservatively. Nevertheless, there is overwhelming support for the early surgical closure of high-output leaks as it emerges that conservative management is failing. If no lymphatic leak is identifiable on reexploration of the neck wound, it is our customary practice to seal the leaking area, covering it with a muscle flap.
Shoulder dysfunction due to spinal accessory nerve injury is thought to affect 25–50% of patients undergoing lateral neck dissection, depending on the extent of that dissection [20,63–65]. Unlike recurrent laryngeal nerve injury, which is quickly recognized clinically and through postoperative laryngoscopy, spinal accessory nerve injury starts out subtle and may take weeks to manifest fully, at which time the patient is no longer hospitalized. Specific neurological examinations are often necessary to make the diagnosis [63–65]. Accessory nerve dysfunction causes the trapezius muscle to weaken, diminishing shoulder abduction and flexion . Many patients with shoulder dysfunction and pain, struggling to resume their former activities of daily life, are unable to return to work . In the first 6 months after the operation, physiotherapy may facilitate the recovery of trapezius muscle function, after which time muscle strength is unlikely to recover further .
A review of the pertinent literature disclosed that the surgical risks of lateral compartment dissection for thyroid cancer are frequently underestimated. There is a dire need for more research using more sensitive detection methods so that the treatment of neurological deficits can be improved. In view of the socioeconomic ramifications of postoperative shoulder dysfunction, affecting as many as 67% of patients , and given the unavailability of effective therapies , the indication for, and the extent of lateral neck dissection for thyroid cancer must be scrutinized weighing oncologic benefits against surgical morbidity.
Lateral neck dissection for metastatic thyroid cancer, owing to the centrifugal orientation of the lymphatic system draining the thyroid gland, is a fairly common procedure. Tumors lodging in the upper thyroid pole may skip the central compartment, spreading directly to the superior lateral nodes (first basin), whereas tumors located in the inferior thyroid pole tend to involve both the central and the inferior lateral (supraclavicular) nodes (first basin). Contralateral lateral neck metastases, in particular in patients with MTC, are associated with mediastinal and distant metastases.
Although dissection of the lateral neck compartment is warranted for clinically involved lateral neck nodes, prophylactic lateral compartment dissections, giving rise to lateral nerve injuries more often than previously thought, should be limited to tumors originating from the upper thyroid pole or thyroid tumors with extensive involvement of the ipsilateral or bilateral central neck compartment. In patients with MTC and preoperative basal calcitonin levels more than 200 pg/ml, a central and bilateral lateral compartment dissection is needed, whereas a central and unilateral lateral compartment dissection would be adequate below that threshold.
Conflicts of interest
This research did not receive any specific grant from any funding agency in the public, commercial, or not-for-profit sector.
The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.
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Papers of particular interest, published within the annual period of review, have been highlighted as:
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