Evaluating the efficacy of the endoscopic thyroidectomy via sternocleidomastoid muscle posteroinferior approach in identifying occult lateral cervical lymph node metastasis
IntroductionOther Section
Thyroid cancer ranks ninth in global cancer incidence and has emerged as the fastest-growing malignant tumor in recent years. By 2030, it is expected to become the second most common malignant tumor among females, with an increasingly younger age of onset (1). Papillary thyroid carcinoma (PTC) is the most common type of thyroid cancer and has a relatively low mortality and good prognosis compared to other common malignancies. However, PTC is prone to lymph node metastasis, and studies have shown that patients evaluated preoperatively for clinical negative lymph node (cN0), the incidence of central cervical lymph node metastasis (CLNM) ranges from 30% to 80% (2), and lateral cervical lymph node metastasis (LLNM) ranges from 18% to 64% (3-5). Patients with LLNM exhibit higher rates of postoperative recurrence and distant metastasis (6).
Preoperative ultrasound and neck enhanced computer tomography (CT) are commonly used to screen for cervical lymph node metastasis, yet their sensitivity (23–67%), specificity (70–79%), and accuracy (70–91%) are limited (7,8). Therefore, a considerable number of cervical lymph node metastasis of PTC cannot be detected before operation. Current guidelines do not recommend prophylactic cervical dissection for PTC patients with a preoperative cN0 assessment (9), resulting in residual cervical lymph node metastasis and increased risk of postoperative recurrence and secondary surgery. Occult lateral cervical lymph node metastasis (OLLNM) refers to negative clinical evaluation and imaging examination (B-ultrasound, CT, magnetic resonance imaging, etc.), but positive intraoperative or postoperative pathological examination of the lateral cervical lymph node (10). This condition is often overlooked by surgeons. Traditional anterior cervical median approach thyroid surgery for lymph node dissection results in a longer incision and prominent postoperative scarring, conflicting with aesthetic considerations. Conventional endoscopic thyroid surgeries, such as oral, axillary, and subclavian approaches, pose difficulties in cervical lymph node dissection.
Our team has developed a novel minimally invasive technique: endoscopic thyroidectomy via sternocleidomastoid muscle posteroinferior approach (ETSPIA). This approach facilitates the removal of latent cervical lymph node metastasis without extending the incision. In this study, we retrospectively analyzed 142 PTC patients who underwent ETSPIA to evaluate its efficacy in clearing OLLNM without increasing patient incision or trauma. Additionally, we investigated the risk factors associated with PTC OLLNM. We present this article in accordance with the TREND reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-24-340/rc).
MethodsOther Section
Patients
A retrospective study was performed on 142 patients diagnosed with PTC who underwent ETSPIA at the Thyroid Head and Neck Surgery Department of Beijing Tongren Hospital, Capital Medical University from November 2022 to June 2024. The patient cohort comprised 43 males and 99 females, aged 22 to 60 years, with a median age of 43 years. All participants were in generally good health, free of significant underlying conditions, and had thyroid nodules detected during routine physical examinations. Preoperative ultrasound assessments of the thyroid and cervical lymph nodes were conducted in our hospital.
Inclusion criteria for the study encompassed: (I) undergoing thyroid surgery for the first time; (II) primary thyroid lesion confirmed as PTC through pathological examination; (III) preoperative imaging indicating a maximum thyroid nodule diameter of ≤4 cm and a maximum lymph nodes diameter of <2 cm. Exclusion criteria were: (I) preoperative thyroid dysfunction or thyroid endocrine disorders; (II) previous history of cervical surgery, radiotherapy, or thermal ablation; and (III) presence of other systemic malignancies. Criteria for PTC cervical lymph node ultrasound included exclusion of secondary lesions, unclear or absent hilar-pulp structure, presence of central microcalcifications, peripheral or mixed blood flow patterns, and cystic changes in lymph nodes.
Comprehensive data on clinical features, pathological findings, and perioperative outcomes were systematically recorded. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This retrospective study was approved by the Beijing Tongren Hospital Ethics Committee (No. TREC2023-xjs07) and informed consent was taken from all of the patients.
Operative procedure
All patients were operated on by the same head and neck surgeon with extensive clinical experience. (I) Body position and incision design. The patient is positioned supine with the head in a neutral midline orientation. A lateral neck incision is made following the natural skin crease, located 1 cm posterior to the sternocleidomastoid muscle, extending from anterior to posterior with a length of 3.5 to 4.5 cm. The transverse cervical nerve, great auricular nerve, accessory nerve, lesser occipital nerve, and external jugular vein are carefully dissected and preserved. A protective sheath is applied to safeguard the incision site. During the operation, nerve monitoring was used in both groups of patients, and the position and function of the recurrent laryngeal nerve could be accurately detected during the operation. (II) No gas injection cavity. The sternocleidomastoid muscle is dissected along its posterior border, extending inferiorly to the point where it attaches to the clavicular head and superiorly to the region where the posterior belly of the digastric muscle converges with the intermediate tendon. Medially and superiorly, the dissection reaches the lateral edge of the superior belly of the omohyoid muscle and the carotid triangle. A retractor is used to elevate the sternocleidomastoid muscle, along with the omohyoid muscle underneath. (III) Expose the thyroid gland. The omohyoid muscle is dissected, and a retractor is placed beneath it to expose the lateral border of the sternothyroid muscle. Depending on the preoperative puncture results, the muscle is either resected or preserved. The ansa cervicalis and its muscular branches are carefully preserved. (IV) Remove the gland. The superior thyroid vessels are dissected and ligated, followed by exposure and preservation of the superior parathyroid gland. The recurrent laryngeal nerve is carefully identified and protected. Subsequently, the middle thyroid vein and inferior thyroid artery and vein are dissected and ligated in sequence, and the thyroid isthmus is divided. (V) Central lymph node dissection. Intraoperative central lymph nodes may be dissected along with the thyroid gland, followed by prelaryngeal, pretracheal, and contralateral central lymph nodes. (VI) Cervical lymph node dissection. Initially, lymph nodes in level III and IIa located medial to the internal jugular vein were excised and sent for intraoperative frozen section analysis as sentinel lymph nodes. If the pathology report indicated positive findings, dissection proceeds to include the lymph nodes in level IIb, located lateral to the internal jugular vein, as well as those in level IV and V. If the results are negative, neck dissection is halted or performed selectively based on preoperative imaging. (VII) Incision suture and drainage. The surgical procedure is shown in Figure 1.
Statistical analysis
The clinical features, pathological features and perioperative data of the patients were summarized. Quantitative data of normal distribution were expressed as mean ± standard deviation, and t-test was used for comparison between groups. The quantitative data of non-normal distribution were expressed as median [interquartile range (IQR)], and Wilcoxon rank sum test was used for comparison between groups. The statistical data were expressed by component ratio and χ2 test was used for comparison between groups. Logistic regression analysis was used to analyze the influence factors of OLLNM. All statistical analyses were performed using SPSS 26.0 (IBM Corp., Armonk, NY, USA), and a P value <0.05 was statistically significant.
ResultsOther Section
Clinical characteristics and surgical outcomes
In this study, 142 patients with PTC successfully underwent unilateral lobectomy and selective neck lymph node dissection via ETSPIA. Detailed clinical characteristics of the patients are presented in Table 1. The median operative time was 3 h 50 min, with a median intraoperative blood loss of 20 mL and a median postoperative hospital stay of 4 days. The median follow-up period was 17 months. During follow-up, none of the patients reported discomfort such as anterior neck pressure or dysphagia. No transient recurrent laryngeal nerve injury-induced hoarseness was observed. Two patients developed chylous leakage, and four patients experienced postoperative numbness in the extremities, all of whom were discharged after standard treatment. Additionally, five patients reported numbness behind the ears, which resolved within a month. None of the patients received 131I treatment postoperatively.
Table 1
Variables | No. of patients [%] |
---|---|
Gender | |
Male | 43 [30] |
Female | 99 [70] |
Age (years) | |
≤45 | 89 [63] |
>45 | 53 [37] |
T stage | |
T1a | 91 [64] |
T1b | 37 [26] |
T2 | 9 [6] |
T3a | 0 |
T3b | 5 [4] |
N stage | |
N0 | 60 [42] |
N1a | 37 [26] |
N1b | 45 [32] |
Tumor location | |
Upper pole | 25 [18] |
Middle | 85 [60] |
Lower pole | 32 [23] |
Tumor number | |
Single | 108 [76] |
Multiple | 34 [24] |
Tumor diameter (cm) | |
≤1.0 | 91 [64] |
>1.0 | 51 [36] |
Capsule invasion | |
Yes | 72 [51] |
No | 70 [49] |
Extrathyroidal extension | |
Yes | 6 [4] |
No | 136 [96] |
Hashimoto’s thyroiditis | |
Yes | 35 [25] |
No | 107 [75] |
Operative time (h) | |
≤4 | 71 [50] |
>4 | 71 [50] |
Blood loss (mL) | |
≤10 | 42 [30] |
>10, ≤30 | 97 [68] |
>30, ≤50 | 3 [2] |
Length of stay (days) | |
≤7 | 99 [70] |
>7 | 43 [30] |
Postoperative complications | |
None | 131 [92] |
Chyle leak | 2 [1] |
Hoarse voice | 0 |
Numbness in hands and feet | 4 [3] |
Numbness behind the ear | 5 [4] |
Cervical lymph node metastasis
The cervical lymph node metastasis status of the 142 patients is detailed in Table 2. Preoperative ultrasound indicated that 117 patients had no cervical lymph node metastasis; 14 patients had CLNM, 10 had LLNM, and 1 patient had both CLNM and LLNM. Postoperative pathology confirmed that 64 patients had no lymph node metastasis, 37 had only CLNM, 12 had only LLNM, and 29 had both CLNM and LLNM. Among the 11 patients whose preoperative ultrasound suggested LLNM (characterized by obscured medulla-hilus structure, unclear lymphatic hilum structure, and unevenly enhanced cortical echo), 8 were confirmed to have LLNM postoperatively (overt LLNM), while 3 showed no cervical side metastasis postoperatively. The most common sites for PTC LLNM were the ipsilateral level III and IV regions, followed by levels II and V, with level I being less common. The results of this study indicate that ipsilateral level III OLLNM was most prevalent in PTC patients, followed by levels II and IV. Thirty-three patients presented with OLLNM, wherein preoperative ultrasound did not suggest cervical side metastasis, but postoperative pathology confirmed cervical side metastasis. This group comprised 19 males and 14 females, with a median age of 42 years. Tumor-node-metastasis (TNM) staging included 18 cases of T1a, 7 cases of T1b, 4 cases of T2, and 4 cases of T3b. Tumors were located in the upper pole of the thyroid in 12 cases, the middle part in 15 cases, and the lower pole in 6 cases. There were 26 cases of solitary tumors and 7 cases of multiple foci, with 4 cases exhibiting extrathyroidal extension. Overall, the accuracy rate of preoperative ultrasound for detecting PTC LLNM was 73%.
Table 2
Lymph node metastasis | No. of patients [%] |
---|---|
Preoperative ultrasound | |
No lymph node metastasis | 117 [82] |
CLNM | 14 [10] |
LLNM | 10 [7] |
Both CLNM and LLNM | 1 [1] |
Postoperative pathology | |
No lymph node metastasis | 64 [45] |
CLNM | 37 [26] |
LLNM | 12 [8] |
Both CLNM and LLNM | 29 [20] |
CLNM, central cervical lymph node metastasis; LLNM, lateral cervical lymph node metastasis.
Factors influencing occult lateral lymph node metastasis
Excluding the 8 cases of overt LLNM, a univariate and multivariate analysis was conducted on the clinical characteristics of 101 patients without LLNM and 33 patients with OLLNM, as shown in Tables 3,4. The univariate analysis indicated that male gender, younger age, higher T stage of the tumor, preoperative ultrasound indicating the tumor located in the upper pole of the thyroid, and extrathyroidal extension were associated with OLLNM (P<0.001, P=0.02, P=0.007, P<0.001, P=0.003 respectively). These factors (gender, age, tumor T stage, tumor location, and extrathyroidal extension) with P<0.05 in the univariate analysis were included in a logistic regression model for multivariate analysis. The results demonstrated that male gender, younger age, preoperative ultrasound indicating the tumor located in the upper pole of the thyroid, and extrathyroidal extension were independent risk factors for OLLNM (P=0.001, P=0.006, P=0.02, P=0.002, respectively).
Table 3
Variables | Lateral cervical lymph node | P value | |
---|---|---|---|
No OLLNM (n=101) | OLLNM (n=33) | ||
Gender | <0.001 | ||
Male | 22 | 19 | |
Female | 79 | 14 | |
Age (years) | 43.50±10.24 | 38.52±9.94 | 0.02 |
T stage | 0.007 | ||
1a | 70 | 18 | |
1b | 26 | 7 | |
2 | 4 | 4 | |
3a | 0 | 0 | |
3b | 1 | 4 | |
N stage | – | ||
0 | 60 | 0 | |
1a | 41 | 0 | |
1b | 0 | 33 | |
Tumor location | <0.001 | ||
Upper pole | 8 | 12 | |
Middle | 69 | 15 | |
Lower pole | 24 | 6 | |
Tumor number | 0.68 | ||
Single | 76 | 26 | |
Multiple | 25 | 7 | |
Tumor diameter (cm) | 0.12 | ||
≤1.0 | 70 | 18 | |
>1.0 | 31 | 15 | |
Capsule invasion | 0.13 | ||
Yes | 55 | 13 | |
No | 46 | 20 | |
Extrathyroidal extension | 0.003 | ||
Yes | 1 | 29 | |
No | 100 | 4 | |
Number of lymph nodes removed | |||
Level II positive | 0 | 0.73±0.88 | |
Level II total | 2.41±2.47 | 5.76±4.17 | <0.001 |
Level III positive | 0 | 0.97±0.81 | |
Level III total | 3.07±3.09 | 6.03±2.54 | <0.001 |
Level IV positive | 0 | 0.21±0.89 | |
Level IV total | 1.22±2.30 | 3.33±3.27 | <0.001 |
Level V positive | 0 | 0.03±0.17 | |
Level V total | 0.05±0.41 | 0.36±0.99 | 0.01 |
Level VI positive | 1.22±2.04 | 2.70±3.11 | 0.002 |
Level VI total | 6.36±4.26 | 6.33±5.02 | 0.98 |
Hashimoto’s thyroiditis | 0.68 | ||
Yes | 25 | 7 | |
No | 76 | 26 |
Data are presented as n or mean ± standard deviation. OLLNM, occult lateral cervical lymph node metastasis.
Table 4
Variables | β | SE | Wald | Exp (β) | P value | 95% CI |
---|---|---|---|---|---|---|
Gender (male) | 2.384 | 0.557 | 18.298 | 10.843 | 0.001 | 3.638–32.318 |
Age | −0.079 | 0.029 | 7.688 | 0.924 | 0.006 | 0.874–0.977 |
Tumor location (upper pole) | 1.823 | 0.762 | 5.717 | 6.189 | 0.02 | 1.389–27.579 |
Extrathyroidal extension | 3.811 | 1.240 | 9.452 | 45.179 | 0.002 | 3.980–512.870 |
OLLNM, occult lateral cervical lymph node metastasis; SE, standard error; Exp (β), odds ratio; CI, confidence interval.
DiscussionOther Section
LLNM is a well-established prognostic factor influencing recurrence and survival in patients with PTC (11). Traditionally, central lymph nodes are considered sentinel nodes for lymphatic drainage in PTC (12), leading both domestic and international guidelines to recommend against prophylactic lateral neck lymph node dissection. Instead, therapeutic dissection is advised when LLNM is confirmed through preoperative assessment or intraoperative frozen section analysis. The dissection typically involves levels II, III, IV, and VB, with the minimal extent including levels II A, III, and IV1. However, previous studies indicate that OLLNM is relatively common in PTC patients. Lim et al. (13) reported an OLLNM incidence as high as 55% in PTC patients undergoing prophylactic lateral neck dissection for ipsilateral CLNM. In our study, postoperative pathology confirmed OLLNM in 25% of patients. Currently, guidelines for unilateral PTC with ipsilateral lateral neck lymph node metastasis, absent other high-risk factors (such as extrathyroidal extension of the primary lesion or lymph nodes, tumor diameter >4 cm, or metastatic lymph nodes ≥3 cm), remain contentious regarding the extent of primary tumor resection. The 2018 guidelines from the Japan Association of Endocrine Surgeons advocate for individualized treatment based on risk stratification, suggesting either unilateral lobectomy or total thyroidectomy depending on prognostic factors and patient conditions. In this study, preoperative imaging did not reveal contralateral thyroid nodules or suspicious contralateral neck lymph nodes. Among the 26 patients with confirmed lateral neck lymph node metastasis, the number of metastatic nodes was relatively low, not exceeding five in any case. According to the 2015 ATA guidelines, such patients may not require postoperative 131I treatment, thus we opted for individualized unilateral lobectomy. Nonetheless, the optimal extent of lateral neck dissection and the necessity for total thyroidectomy in patients with lateral neck lymph node metastasis remain debated. Further research is needed to balance minimizing tumor residuals or recurrence with reducing unnecessary surgical trauma.
Thyroid surgery involving lateral neck lymph node dissection benefits from ETSPIA for several reasons: compared to traditional anterior cervical approaches, ETSPIA offers aesthetic incisions and minimal tissue trauma. Conventional open surgery incisions, such as “L” shaped, “U” shaped, and lower cervical apron-shaped large arc incisions, tend to be long, resulting in prominent postoperative scars that significantly affect the appearance of the neck (14). In contrast, the ETSPIA incision is located within the natural skin folds on the lateral neck, experiencing lower tension and more even fat distribution, promoting better wound healing. Moreover, the incision can be concealed beneath the collar, ensuring postoperative aesthetics (Figure 2). Additionally, open incisions require opening the enveloping fascia, which can cause postoperative anterior cervical pressure, numbness, and discomfort during swallowing. ETSPIA accesses the thyroid surgical area through the deep intermuscular spaces of the strap muscles, avoiding the opening of the enveloping fascia, significantly reducing tissue adhesion in the anterior cervical region, and lowering the risk of transverse cervical nerve injury, thereby significantly alleviating postoperative cervical discomfort. ETSPIA allows for radical dissection of lateral neck lymph nodes compared to other mainstream endoscopic thyroid surgeries. This approach begins with the dissection of lymph nodes in areas III and IIA on the medial side of the internal jugular vein, sending them for intraoperative frozen section analysis as sentinel lymph nodes. If positive, dissection continues to lymph nodes in areas IIB, IV, and V on the lateral side of the internal jugular vein. This method ensures a shorter dissection route with minimal trauma, determining the extent of lateral neck lymph node dissection based on sentinel node results, thus preventing recurrence due to occult metastatic lymph nodes and avoiding unnecessary dissection in all patients, which would increase trauma. Additionally, ETSPIA offers a direct view of the thyroid lobes, accessing the thyroid’s posterior lateral capsule and better protecting the recurrent laryngeal nerve, thyroid suspensory ligament, and superior thyroid artery, reducing the risk of damaging critical structures (15). In this study, no patients experienced transient recurrent laryngeal nerve injury leading to hoarseness postoperatively. In summary, ETSPIA adheres to the new concept of performing endoscopic surgery through natural tissue spaces, characterized by concealed incisions, shorter pathways, minimal tissue trauma, rapid postoperative recovery, and ease of operation for surgeons. It enables radical dissection of lateral neck lymph nodes, representing a truly minimally invasive surgery. This study investigates the value of ETSPIA in treating OLLNM while also analyzing associated factors. PTC manifests differently across gender and age groups, although more prevalent in females (16), PTC tends to be more aggressive in younger males. Girardi et al. (17) validated that, despite a lower incidence of PTC in males, they exhibit a higher propensity for LLNM, consistent with our findings. In our study, younger age emerged as another risk factor for PTC OLLNM. Patron et al. (10) analyzed 173 PTC patients with OLLNM and found that age below 45 years was a risk factor for LLNM. Sugitani et al. (18) hypothesized that this could be due to higher cellular metabolic activity leading to increased lymph node response, though this remains inconclusive. Additionally, our data indicate a significant increase in OLLNM risk when preoperative ultrasound suggests tumor localization in the upper pole of the thyroid gland. In this study, 25 cases had tumors in the upper pole, with 17 exhibiting lateral neck metastasis (68%) and 14 exhibiting central region metastasis (56%). Weng et al. (19) found that PTC in the upper thyroid can lead to skip metastasis to lateral neck lymph nodes, without central lymph node involvement. Tumor cells in the upper pole may be transported via lymphatic vessels to lateral lymph nodes near the superior thyroid artery, facilitating skip metastasis to regions II and III (20,21). Therefore, when preoperative ultrasound indicates tumor presence in the upper pole, lateral neck lymph node dissection is recommended to reduce the likelihood of recurrence and subsequent surgeries due to lymph node metastasis. Moreover, several studies have identified extrathyroidal extension of the tumor as an independent risk factor for LLNM (10,17). In our study, five PTC patients exhibited extrathyroidal extension, with postoperative pathology confirming OLLNM in four cases. The risk factors for OLLNM identified in this study can be ascertained preoperatively and intraoperatively, aiding in the early detection of high-risk PTC patients.
However, ETSPIA has some technical challenges and limitations. For large lesions or thyroid lobes, the limited operating space increases the surgery’s difficulty, requiring careful preoperative evaluation. This approach navigates between the deep surface of the sternocleidomastoid muscle and the carotid sheath, posing a risk of injury to the carotid sheath and hypoglossal nerve loop. This study has limitations, including a small sample size and short follow-up period, and single-center research may introduce errors in the sensitivity and accuracy of preoperative ultrasonographic evaluations. In the future, we plan to expand the case cohort and lengthen the follow-up period to compare ETSPIA with open and other endoscopic thyroidectomy techniques, aiming to comprehensively assess the role of ETSPIA in PTC treatment.
ConclusionsOther Section
Our team has pioneered ETSPIA, utilizing natural tissue spaces to thoroughly clear occult metastatic lateral neck lymph nodes. Additionally, we found that male gender, younger age, tumors located in the upper pole of the thyroid, and extrathyroidal extension are significantly associated with OLLNM, providing valuable insights for the broader application of the ETSPIA. This approach ensures radical thyroid cancer treatment while maximizing postoperative aesthetics and comfort, demonstrating significant clinical application value.
AcknowledgmentsOther Section
Funding: This work was supported by Beijing Hospital Management Center “Ascending the Peak” Talent Training Program (No. DFL20220201).
FootnoteOther Section
Reporting Checklist: The authors have completed the TREND reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-24-340/rc
Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-24-340/dss
Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-24-340/prf
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-24-340/coif). The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This retrospective study was approved by the Beijing Tongren Hospital Ethics Committee (No. TREC2023-xjs07) and informed consent was taken from all of the patients.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
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