Among patients with RLN invasion in our cohort, 22.1% (17 of 77) were invaded by metastatic lymph nodes. This rate was higher than that reported in a previous study [6], possibly because of the inclusion of different groups of patients. The imaging characteristics of ETE in conventional ultrasonography have been evaluated and thoroughly discussed [7, 8]. However, in addition to primary thyroid carcinoma, lesions in metastatic lymph nodes can also spread outside the lymph node capsule and invade perinodal soft tissues. Hence, the risk of surrounding tissue invasion (e.g., RLN, jugular vein, and esophagus) remains uncertain for patients with lymph node metastases, even after assessing primary thyroid carcinoma. Over half (9 of 15) of the cases showed no signs of ETE, with the RLN being the only tissue invaded. Given its location in the central compartment and its long course, the RLN is more commonly invaded than other perinodal tissues.

The risk of ENE increases with the number and extent of lymph node metastases [4]. Two-thirds of the patients had multiple thyroid lesions, with most (13 of 15) having lesions with a diameter greater than 1 cm and more than half (9 of 15) having metastases to lateral cervical lymph nodes. Limited by the retrospective study design, most of the images of the metastatic lymph nodes invading the RLN were unavailable, preventing measurement of the diameters of the involved lymph nodes. A study reported that nearly half of the lymph nodes with ENE were less than 1 cm [9]. However, the criterion for ENE in this study was microscopic ENE (mENE). The presence of mENE has emerged as an independent prognostic factor [3, 4, 10], suggesting further modifications to the staging systems for lymph node metastases. Although the pathological criteria for mENE remain controversial, the criteria for gENE and gETE were established via intraoperative inspection, as lymph nodes or thyroid lesions could not be removed from adjacent soft tissues through blunt dissection. Based on the controversies and the possibility of false-positive results, intraoperative findings are increasingly valued in risk systems of thyroid carcinoma [11]. Another reason for adopting the gENE criteria in this study was that the outcomes of the RLNs were more related to intraoperative inspections. Difficulties and limitations persist in ultrasound scanning of lymph nodes in the central compartment [12]. One of the two missed cases on preoperative ultrasonography underwent computed tomography, revealing metastatic lymph nodes with a maximum diameter of 1.4 cm, and eventually underwent successful R1 resection. The other missed case failed R1 resection and underwent R2 resection with a residual tumor dorsal to the RLN. The diameter of the primary thyroid carcinomas in both cases was > 2 cm. These findings suggest that careful scanning of the central compartment is essential in patients with advanced tumor stages. Special attention should be paid to the paratracheal space of patients with suspected lymph node metastases.

One patient was initially managed with active surveillance and presented with thyroid carcinoma less than 1 cm in diameter and an intrathyroidal location. However, multiple enlarged lymph nodes with indistinct structures were found one year later. Despite successful excision of lymph nodes from the epineurium, radioactive iodine therapy followed by total thyroidectomy was inevitable in a 33-year-old female patient. Although active surveillance is accepted as a favorable management strategy for patients with a low risk of PTC, disease progression occurs in a certain number of patients [13, 14]. Moreover, the high incidence of lymphatic metastasis in PTC requires radiologists to pay extra attention to the paratracheal space. Although lymph node metastases of PTC were not associated with survival, ENE to RLNs could significantly affect the management and quality of life of patients with PTC. Only a small number (2 of 15) of RLN-invaded cases presented with vocal cord paralysis preoperatively. One patient showed normal vocal cord mobility during fiberoptic laryngoscopy. The low incidence of vocal cord paralysis and abnormal results of laryngoscopy in patients with RLN invasion highlights the value of ultrasonography in assessing the anatomical integrity of the RLN [15]. Promising results have been obtained regarding the relative positioning of thyroid lesions and RLNs [5, 7].

Based on the high resolution of ultrasonography for evaluating metastatic lymph nodes, the visualization of adjacent RLNs was reviewed. This appears to be the first study to evaluate the clinical and imaging characteristics of RLN invasion by ENE in patients with thyroid carcinoma. In contrast to the typical sites of RLN invasion by primary thyroid carcinoma, two-thirds of RLNs were invaded by metastatic lymph nodes located inferior to the thyroid, reflecting the distribution of lymph nodes in the central compartment. More lymph nodes were located inferior to the thyroid than near the larynx entrance. Moreover, the left-sided location of the esophagus makes lymph nodes posterior to the RLN more common on the right side [16]. This also explains why the right RLNs are more commonly affected in patients with RLN invasion by ENE. Preserving the integrity of RLNs is critical for patients’ long-term quality of life. Both patients who underwent neurectomy developed permanent vocal cord paralysis. One patient underwent a neurectomy followed by immediate ansa cervicalis-RLN anastomosis, resulting in partial relief of hoarseness after surgery. This highlights the importance of not only preventing anatomical integrity but also employing precise surgical techniques for the dissection and reconstruction of invaded RLNs to support vocal cord function recovery [17]. The other patient who underwent a neurectomy had an MTC histological type. Unfortunately, the aggressive nature of the tumor necessitated radical resection, which precluded the use of RLN reconstruction techniques. Hence, to properly manage patients with RLN invasion, decisions should balance oncological outcomes and function preservation. The relationship between R2 resection and recurrence in patients with RLN invasion remains controversial [6, 18]. The two recurrent lesions in this study were both in the lateral neck. No recurrence was found among the three patients who underwent R2 resection. Further randomized controlled studies with long-term follow-up are warranted.

This study had some limitations. First, the retrospective design limited the accessibility of proper ultrasonographic images. Second, given that two-thirds of the cases preserved the integrity of RLNs, the pathological diagnosis of RLN invasion by ENE was insufficient due to a lack of RLN specimens resected. Third, the small number of enrolled patients and the short follow-up period made the oncological results insufficient. However, this study identified the clinical and imaging characteristics of gross RLN invasion by ENE in patients with thyroid carcinoma. We believe that this study provides preliminary insights into central compartment evaluation.