Papillary thyroid carcinoma (PTC) is the most common endocrine malignancy, and accounts for nearly 90% of differentiated thyroid carcinomas (1). Lymph node (LN) metastasis usually develops in PTCs, with a reported incidence of up to 90% (2–4). Routine central neck LN dissection is required for all PTC patients in China, while lateral neck dissection is performed for pathologically positive lateral LN (5).

Excision of LNs located between the sternocleidomastoid and sternohyoid muscles (LNSS) is often overlooked because of it is located in the suprasternal space and falls outside the neck levels VI and level II–V (6–10). Since Sun et al. (6) first described the metastasis pattern of LNSS, other researchers have continued to emphasize the significance of LNSS dissection (7–10). The rate of LNSS metastasis varies from 7.4% to 22.6%, yet the risk factors for LNSS metastasis remain unknown. This study aimed to evaluate the association between clinicopathologic variables and LNSS metastasis to clarify the necessity of LNSS dissection in PTCs.

The most important finding in the current study was that although nearly one third of the patients had LNSS, LNSS metastasis was relatively uncommon. It was most likely to occur with the T3/4 tumors or along with level IV metastasis simultaneously. The rate of LNSS metastasis was found to be low and routine dissection was unnecessary. However, the excision of LNSS was required if there was a presence of advanced stage tumors or LN metastasis in level IV.

The suprasternal space, also known as Burns space, is a narrow interval between the superficial and deep layer of the cervical fascia, located above the manubrium of the sternum. It contains the sternal heads of the sternocleidomastoid, the lower portions of the anterior jugular veins and their transverse connecting branch as well as a small quantity of areolar tissue (12). LNSS was anatomically a part of this space (6–10, 13); however, according to the official definition of level III-VI (14), LNSS does not belong to any of these groups. Moreover, owing to the developmental variation, LNSS is not always present. Song et al. (7) noted LNSS in 75.8% of 264 neck dissection samples, while Hao et al. (8), Sun et al. (9), and Zhang et al. (10) reported LNSS in about 70% of their patients. The incidence was apparently lower than reported in our study. Usually, the detection rate of LNs is associated with a number of factors including the pathologist’s ability to identify the LNs, the surgeon’s ability to dissect the LNs, and the level of dissection (15). It was noted that the size of the LNSS in the current study was very small, representative of the eligibility of our surgeons and pathologists. Thus, it is reasonable to conclude that other factors may account for this variation, such as differences in the study design and inclusion criteria. Moreover, we might be the first to depict the small size of LNSS, which is not easily detected in a CT scan, resulting in the frequent neglection of this special group.

There is a paucity of studies on the metastasis of LNSS and to our knowledge, only five published studies have focused on this issue (6–10). Sun et al. (6) were the first to describe positive LNSS in 22.6% of their 115 neck dissection samples from 115 patients. Consistent with our study findings, Song et al. (7) reported a 17.8% rate of LNSS metastasis in 234 PTC patients undergoing 264 neck dissections, while metastatic incidences of 7.4%, 23.5%, and 14.3% were reported by Hao et al. (8), Sun et al. (9), and Zhang et al. (10), respectively. These findings indicated that the rate of LNSS metastasis was relatively low, raising the important question of when LNSS should be resected.

Predictors for LNSS metastasis remain unclear. Based on a study comprising 115 patients, Sun et al. (6) found a significant association between LNSS metastasis and the level III and level IV nodal metastasis, the lateral LN metastasis, and a primary site in the inferior pole. However, the authors did not perform a multivariate analysis to confirm the independence of these factors. In another study consisting of 264 neck dissections from 234 patients, the authors noted that age over 45 years, a tumor located in the inferior lobe of thyroid, LN metastasis at level IIb, and LN metastasis at level III were all independent metastatic risk factors for LNSS (7). The role of level IIb metastasis was not clear. The rate of level IIb metastasis in PTC was usually very low, thus the routine dissection of level IIb was not deemed to be necessary. However, resection of level IIb was indicated if there were positive LNs in more than three levels (16). Additionally, because of the anatomical distance between level IIb and LNSS, it was hard to assess causality. Sun et al. (9) confirmed the independence of the original tumor size and level IV nodal metastasis in increasing the risk of LNSS metastasis. All the findings emphasized the significance of level IV metastasis; however, they failed to identify the risk as per the number of positive LNs. Cervical LNs with metastasis >6 were associated with an elevated risk of LNSS metastasis (8). Moreover, the current study reiterates the fact that the risk of LNSS metastasis was significantly increased when there were more than two positive LNs in level IV.

Tumor stage was another important predictor. Usually, thyroid LNs only drain to deep cervical LNs, but rarely metastasize to superficial cervical LNs (17). However, advanced stage tumors can invade peripheral tissues such as anterior cervical muscles; cancer cells can then cause LNSS enlargement through the superficial cervical lymphatic drainage system. This viewpoint was confirmed by Zhang et al. (10), who reported that 88.9% of the PTCs with strap muscle involvement had LNSS metastasis, a rate higher than the 19.4% observed in PTCs without strap muscle involvement. Additionally, pre-laryngeal LNs are considered to have communicating branches with superficial cervical lymphatic drainage systems (18). However, we failed to identify the effect of level VI metastasis on LNSS metastasis in this study.

The limitations of the current study must be acknowledged: the prognostic value of LNSS was not analyzed because the follow-up data was not included.

In summary, the rate of LNSS metastasis was low, routine dissection was unnecessary. However, the excision of LNSS was required if there was a presence of advanced stage tumors or LN metastasis in level IV.

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

The study was approved by Xi’an Jiaotong University Institutional Research Committee. The participants were asked to sign an informed consent form. The patients/participants provided their written informed consent to participate in this study.

The conception and design of the work: YZ and LR. The collection and analysis of the data: YZ and LR. The interpretation of the statistic results: YZ and LR. Manuscript writing and revision: YZ and LR. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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