Concerns in patients undergoing neck dissection surgery

KEYWORDS:

• Papillary thyroid carcinoma
• lymph node dissection
• neck nodes metastases
• central neck dissection
• lateral neck dissection
• reoperative lymph node dissection

Lymph node involvement is common in patients with papillary thyroid carcinoma (PTC) and it may negatively affect recurrence rate and, probably, survival [1].

Lymph node neck dissections are demanding and challenging operations associated with several possible complications as many anatomic structures are at risk during the surgical dissection in a relatively small operative field. Trachea, esophagus, laryngeal nerves, and parathyroid glands are extensively exposed during central neck dissection (CND), moreover, when a lateral neck dissection (LND) is performed, internal jugular vein, common carotid artery, vagus, hypoglossal, spinal, phrenic nerves, sympathetic trunk, and brachial plexus could be at risk of injury.

The knowledge of surgical techniques, anatomic landmarks, nomenclatures, and classifications both of the lymph node levels and of the surgical procedures is essential to offer the best surgical option to PTC patients and to obtain homogeneous data to compare literature results [2,3].

Some concerns still exist regarding the indications and the extension of lymph node dissection in PTC both for CND and LND [1].

CND (level VI) is mandatory when macroscopic central neck nodal involvement is found at preoperative work up or during the surgical exploration [1,4–6].

In patients with clinically node negative (cN0) PTC the role of prophylactic CND remains matter of debate [1,4–9]. Multifocal disease and extracapsular tumor invasion have been suggested as potential risk factors for occult nodal metastases in PTC [5,6]. Possible risk factors included also age, sex, and tumor size [5,6]. On this topic, the studies available report discordant results, probably because of the heterogeneous patients’ populations concerning operative and clinicopathologic features (prophylactic vs. therapeutic CND, clinical unifocal vs. clinical multifocal PTC, unilateral vs. bilateral CND) source of uncontrolled bias [6]. In our prospective series of 186 consecutive clinically unifocal cN0 PTC patients (unpublished data) who underwent total thyroidectomy plus prophylactic bilateral CND, we observed that only extracapsular invasion and microscopic multifocal disease were independent risk factors for central neck nodal metastases.

Furthermore, histological variants of PTC have been advocated as possible risk factors for central neck nodal metastases. A lower incidence of nodal metastases in follicular variant of PTC when compared with classic PTC has been observed [10]. According with these results in our retrospective series of 1737 patients with a diagnosis of follicular variant of PTC or classic PTC, we observed a lower incidence of nodal involvement in follicular variant of PTC but no differences between these histological PTC variants regarding risk factors of central neck nodal metastases. We think that the follicular variant PTC seems associated with a lower incidence of nodal metastases presumably because of the higher rate of incidental diagnosis and subsequent Nx staging.

To date there are no evidence to suggest unequivocal preoperatively available clinical parameter as reliable predictor of nodal disease in cN0 PTC.

Prophylactic CND is associated with lower postoperative serum thyroglobulin, allows to improve accuracy in staging and selecting patients for radioiodine ablation (not all occult nodal metastases are micrometastases – ≤2 mm – without clinical relevance) and to reduce the risks of reoperation for recurrence. Conversely, one of the main argument against is the higher risk of complications, namely hypoparathyroidism and laryngeal nerve injuries [4–6,11]. In order to reduce the complications in recent years, a more limited (ipsilateral) CND (IpsiCND), including elective removal of pre-laryngeal, pre-tracheal, and the paratracheal nodes on the side of the tumor, was proposed in patients with clinical unilateral PTC [11]. Comparative studies have suggested that IpsiCND may be an effective alternative option to bilateral CND for cN0 PTC, because of the similar short-term oncologic outcome and the lower risk of postoperative complications, namely transient hypocalcemia [11]. On the other hand, IpsiCND implies the risk of overlooking contralateral metastases [11]. Since isolated contralateral metastases are exceptional, it has been suggested that frozen section examination (FSE) on the ipsilateral central neck nodes can be used to intraoperatively assess the ipsilateral nodal status and to subsequently modulate the extension of the prophylactic CND [12]. We have found that FSE has a sensitivity, specificity, and overall accuracy of 80.7%, 100%, and 90%, respectively, in detecting occult ipsilateral central neck metastases in clinically unifocal cN0 PTC. Most of the false negative results we observed were obtained in case of micrometastases, which are usually of little clinical significance [12].

We have recently confirmed this results in a prospective study [13] including 100 patients and comparing IpsiCND plus FSE and bilateral prophylactic CND in clinically unifocal cN0 PTC. In the IpsiCND group removed lymph nodes were sent for FSE. If FSE was positive for lymph node metastases, a bilateral CND was accomplished. We found no significant difference between IpsiCND plus FSE and bilateral prophylactic CND groups in terms of accuracy of N staging and short-term oncologic outcome [13]. Additionally, more patients in the bilateral prophylactic CND group experienced transient hypocalcemia than in the IpsiCND plus FSE group, this result was not statistically significant but can be explained by the small number of patients included and, above all, by the fact that IpsiCND plus FSE group included also patients who underwent bilateral CND after FSE positive for occult nodal metastases [13]. Probably comparative studies with larger series of patients and longer follow-up data are necessary to completely validate this intraoperative decision-making approach but, based on our results, we think that in clinically unifocal cN0 PTC routine IpsiCND plus FSE of the ipsilateral nodes could be a valid alternative to prophylactic bilateral CND since it allows accurate staging and it may reduce morbidity.

Regarding the LND most guidelines recommend that LND should be performed only with therapeutic intent for known disease and not for prophylactic purpose [4,5,14,15]. Despite this consensus regarding the indications, the extension of therapeutic LND is still debated [4,5,14,15].

Selective compartment-oriented LND, including levels IIa-III-IV-Vb, is considered the standard treatment for PTC with LN metastases. However, more limited approaches (i.e. level III and IV dissection) have been proposed. Moreover, some authors have been suggested that in PTC metastatic spread to the lateral neck can be influenced by the intrathyroidal location of the primary tumor [14,15]. In our recent prospective series of 159 PTC patients (unpublished data) with clinical evidence of lateral neck nodal metastases at level III and/or IV (without clinical evidence of nodal metastases at level II and/or V) who underwent selective compartment-oriented LND, including levels IIa-III-IV-Vb, we observed nodal metastases at level IIa, III, IV, and Vb in 49.7%, 73.7%, 74.3%, and 14.0% of patients, respectively. Furthermore, our results showed that the pattern of metastatic lateral neck nodal spread was independent from intrathyroidal tumor location (superior, middle, and inferior aspect of the thyroid lobe). Moreover in our retrospective series of patients who underwent therapeutic primary or reiterative LND for PTC, we observed that limited LND and surgery performed at non-referral centers were non-tumor-related independent risk factors for recurrence following therapeutic LND for PTC.

Basing on our experience and in absence of high level of evidence, we think that to date patterns of lateral neck lymphatic spread do not justify limited LND approaches and that selective compartment-oriented LND, including levels IIa-III-IV-Vb, remains the standard treatment for PTC with lateral neck nodal metastases.

Unfortunately, about 15–30% of the PTC patients will develop recurrent nodal disease after the initial surgical treatment requiring resection of cervical recurrences with curative intent and in order to prevent locoregional complications [16]. In these cases, the complicated neck nodal surgery became challenging. One should keep in mind that secondary surgery in the central compartment is always a reoperation and that secondary surgery in the lateral compartment may be ‘virgin’ or reiterative depending upon whether prior lateral neck node surgery has been performed [16]. The reoperations are demanding procedures theoretically associated with an increased risk of complications. Indeed, the presence of dense scar tissue and the disruption of the normal anatomic relationships can make difficult the identification and preservation of the recurrent laryngeal nerves, parathyroid glands, etc. Since such technical difficulties, the surgeon should have accurate documentation of previous surgical procedure(s) (namely surgical and pathological reports), accurate preoperative imaging and extensive experience in neck surgery. Surgical strategy should be adequately planned to reduce the risk of potential complications.

In a case-control study including 82 patients, we evaluated if reoperative CND implies an increased postoperative morbidity and we aimed also to verify the effectiveness of the surgical resection of reoperative CND. We observed no significant difference between the reoperative and the control groups concerning postoperative complications rate and oncologic outcome concluding that in high volume centers reoperative CND is as safe and as effective as primary CND in patients with PTC. On the other hand, it is not doubtful that reoperative neck nodal procedures are challenging operations, especially for not experienced surgeons. For this reason, we think that patients who require reiterative neck surgery should be referred preferably and if feasible to high volume tertiary centers in order to reduce the risk of potential complications achieving an optimal locoregional control of the disease [16].

Summary recommendations

• – Central neck dissection

  • ∘ clinical multifocal PTC /extracapsular invasion /cN1: bilateral central neck dissection

  • ∘ clinical unifocal PTC and cN0: ipsilateral central neck dissection with FSE, if positive bilateral central neck dissection

• – Lateral neck dissection

  • ∘ cN1: in case of evidence of unilateral or bilateral lateral neck nodal metastases unilateral or bilateral selective lateral neck dissection including levels IIa-III-IV-Vb

  • ∘ cN0: no prophylactic lateral neck dissection

Declaration of interest

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.

Additional information

Funding

No funding to declare.